We found weak support for complementarity of the direction of vigilance between the two associating tamarin species. Only the comparison between SSG and MSG of the same size supported our prediction (comparison B, prediction 2), and that was true only for individuals in smaller groups during resting where individuals in the population that never associated with other species looked downwards more than individuals in MSG (Table 2, Fig. 3). In larger groups, there were no differences between MSG and SSG of the same size, which could imply that heterospecifics play a more important role in smaller groups, but data on more groups would be needed for firmer conclusions.
The idea of the division of labor was further supported by the analysis of directions of vigilance within groups (Table 2). Mustached tamarins in all groups tended to look downwards more than upwards, but while the difference at EBQB was of only a few percent and could hardly have an ecological significance, it was about twofold at PI. It seems that tamarins in the population that has no contact with other primate species compensate for the absence of heterospecifics by increased scanning downwards.
However, comparisons of vigilance behavior in cases A and C gave results that were less straightforward. Individuals that were temporarily out of association (case A) increased their total vigilance as predicted by the group size effect, but that was due to horizontal, not downward, scanning. A similar behavioral response was observed when comparing individuals in the group with a higher percentage of conspecifics with those in the group with a smaller percentage of conspecifics (case C), although we predicted no difference in total vigilance levels in groups of the same size. We offer three explanations for why horizontal scanning increases in these two cases. First, non-antipredator functions such as food searching and especially social vigilance are probably much more included in horizontal than in upward or downward scanning because conspecifics are usually found at about the same height as the focal individual. Having other functions in addition to antipredator detection is probably also the reason why horizontal scanning takes up much more of animals' time than looking upwards or downwards (Table 2). In a group with more conspecifics (comparison C), there is probably an increased need for social vigilance. Our previous study suggests that, while the major function of vigilance is predator-related, the most probable reason for monitoring conspecific group members in mustached tamarins is maintaining group cohesion (Stojan-Dolar and Heymann 2009). This certainly becomes more challenging with an increased number of conspecifics in the group. Yet, this interpretation does not explain why horizontal scanning increases when mustached tamarins are temporarily found out of association (comparison A). Other functions of social vigilance such as avoiding food stealing or aggression that are usually mentioned in studies on other species (e.g., Jones 1998; Steenbeek et al. 1999; Hirsch 2002) have not been found in the relatively non-aggressive society of these cooperatively breeding primates.
Second, due to the arboreal nature of neotropical felines callitrichids might increase horizontal or even upward scanning as a response to terrestrial predators (Barros et al. 2008). Neotropical felines and tayras can climb trees occasionally (Emmons 1987; Wang 2002), and the absence of the lower-living species certainly increases the probability that a predator climbing up a tree will remain unnoticed. This may be why mustached tamarins in both temporary and permanent SSG were found at greater heights than those in MSG (even though the forest at PI was actually lower than at EBQB), which gives an impression that this is a general reaction to the absence of heterospecifics that is not conditioned with the type of predators. The height of saddleback tamarins, on the other hand, is not affected by the presence or absence of congeners (Buchanan-Smith 1999), which may mean that they are more specialized to their specific niche and/or that there are antipredator benefits of living in lower forest strata.
And third, since mustached tamarins are found at higher levels in the forest and raptors are ambush predators that often perch within canopies (Rettig 1978; Robinson 1994), it might not be necessary to elevate the gaze for more than 45° in order to detect them—especially since monkeys even further increase their height when in SSG. Horizontal scanning might therefore also have an important role in detection of aerial predators, and it has been understood as such also in some other vigilance studies (Peres 1993; Bshary and Noë 1997). Increased vigilance against raptors in a group of the same total size but with fewer heterospecifics (case C) or in the absence of heterospecifics (case A) can imply that lower-ranging heterospecifics have a complementary role that cannot be compensated by adding additional conspecifics, not only in the detection of terrestrial but also aerial predators. This might occur because the lower-ranging saddlebacks see the upper levels of the forest and the sky from a different angle—a fact that could be important in a habitat with dense vegetation. But it can also emerge simply because the benefits of contributing vigilance in such a group are greater than in a group with more heterospecifics. In this case, contributing vigilance can be seen as a case of a component tragedy of the commons, where vigilance is a social good (Rankin et al. 2007). When the percentage of conspecifics is high, it is more likely that a predator would take a conspecific than when the percentage of conspecifics is low. Here, it is important to note that tamarins live in a highly cooperative society where reproductive success depends heavily on help from conspecifics (Caine 1993; Garber 1997) and where the degree of relatedness within the group is relatively high (Huck et al. 2005). Hence, if a predator kills a conspecific, this can have direct consequences for the fitness of other individuals—they lose a helper who is also quite likely to be a close relative. The associating species therefore both contribute vigilance to improve group safety, but the ratio between costs and benefits of contributing depends on the percentage of conspecifics in MSG. When the benefits/percentage of conspecifics are high, they tend to contribute more; when the benefits/percentage of conspecifics are low, they tend to free-ride more. However, vigilance can never drop under a certain level because individuals also increase their personal safety by being watchful.
In addition to that, individuals that are temporarily out of association (case A) are probably more vigilant already due to the group size effect. However, it remains unusual that upward scanning that certainly also serves detecting birds of prey did not increase.
A general observation based on our results is that the two populations did not respond in the same way to changes in group size and species composition. Tamarins from EBQB reacted by increasing total vigilance due to increased horizontal scanning, whereas the comparison with same-sized groups from PI revealed either no differences in vigilance or the expected changes in downward scanning (Fig. 1). Summarizing the above-described mechanisms, we may explain the observed results as follows: In case A, individuals that are temporarily out of association increased their vigilance due to the group size effect, the absence of the lower-ranging species, and/or increased benefits of contributing vigilance. In case B, individuals in the smaller groups from PI increased their vigilance against terrestrial predators due to the permanent absence of the lower-ranging species. And in case C, individuals in the group with a higher percentage of conspecifics increased their horizontal scanning due to an increased need to monitor conspecifics in order to maintain group cohesion and/or increased benefits of contributing vigilance.
It is difficult to speculate about the reasons for these mechanisms to act only under certain circumstances. However, there are two major differences between the populations that could give some clue as to why this occurs. First, the forest on PI is less dense and lower than at EBQB, and as a consequence it is possible that there are different species of birds of prey present that might use different attack tactics. By recording alarm calls, we measured perceived predation risk, but we were not able to identify species that actually prey upon tamarins. Birds or conspecifics within the canopy are easier to detect in conditions of lower vegetation density, and therefore, benefits of increasing horizontal vigilance in order to monitor conspecifics or to detect aerial predators are not the same as at EBQB. Furthermore, there are no felines or tyras on the island, which means that horizontal scanning is unlikely to be intended to detect terrestrial predators. However, terrestrial threat is not absent as monkeys perceive dogs as potential predators. And second, tamarins at PI do not have any experience with other primate species, while animals at EBQB have had an opportunity to learn to adjust their vigilance according to the group species composition. Being only temporarily out of association or having a lower percentage of heterospecifics in MSG might elicit different reactions than living permanently in SSG and not having any experience with other primates.
Comparison with results of other studies on primate MSG that are analogous to our comparison A also implies that there is no uniform explanation for changes of vigilance patterns under different MSG/SSG conditions (Table 3). Individuals in different combinations of African cercopithecids have been observed to increase, decrease, or not to change their total vigilance at all when they are temporarily found in SSG, which appears to depend on which species they associate with (Cords 1990; Chapman and Chapman 1996; Bshary and Noë 1997; Treves 1999). With regard to callitrichids, a study on captive red-bellied (S. labiatus) and saddleback tamarins revealed that higher-ranging red-bellied tamarins increased “scanning” when they were housed without saddlebacks (Buchanan-Smith and Hardie 1997; Hardie and Buchanan-Smith 1997). Since the definition of “scanning” in that study included also looking sideways, these results might be consistent with our findings.
Mixed results are not uncommon in vigilance literature. The effects of sex, age, distance to cover, and also group size on vigilance vary greatly across different species and studies (reviewed in Caro 2005; Beauchamp 2008). Inconsistent results from studies on different species could occur due to differences in predation pressure between sites and species, differences in typical group sizes of different species, but also differences in methodology employed by different researchers. In order to facilitate comparison between species and populations, future studies should differentiate between all three possible directions of vigilance and take into account that vigilance can have a social as well as an antipredator component that might show different patterns (Klose et al. 2009). Different studies also operate with different measures of vigilance (percentage of time vigilant, frequency/duration of vigilance bouts) that appear to give different results (e.g., Trouilloud et al. 2004; Beauchamp 2008).
To sum up, we found indications that associating tamarin species in MSG might complement each other in the direction of vigilance, but the division of labor alone does not satisfactorily explain all the findings. There appear to be other mechanisms at work that define how direction of vigilance changes with group size and species composition. However, this does not directly contradict the notion that heterospecifics have a complementary role in antipredator strategies of MSG. The two species notice different predators already because they live in different forest strata (Gautier-Hion et al. 1983; Peres 1993) and might additionally complement each other by seeing the same predators from different angles; therefore, additional adjustments in the direction of vigilance may not always be necessary. In this case, division of labor between species is still very important, it just does not occur due to differences in the direction of vigilance but rather due to vertical stratification per se. Interestingly, increasing the height in the forest appears to be a more uniform reaction to the absence of heterospecifics than changes in vigilance patterns. Data on more groups and populations and on responses of lower-ranging saddleback tamarins would be needed to gain clearer insight into mechanisms and ecological relevance of complementarity of antipredator behavior in species participating in MSG.