Olfaction and Other Chemical Senses
Physiological and morphological data suggest that the term “microsmatic” may not be a valid descriptor of primates (Laska et al., 2000; Smith and Bhatnagar, 2004; Smith et al., 2004, this issue). All primates possess at least one olfactory system: a main olfactory system (MOS) and, in numerous primates, a vomeronasal (accessory olfactory) system (VS). The roles of these systems in primates are poorly understood because a functional VS is absent in catarrhines and because its function is uncertain in haplorhines (Bhatnagar and Meisami, 1998; Smith et al., 2001; Dennis et al., 2004, this issue). In mammals generally, the sense of smell (olfaction) is mediated through the MOS, which is specialized to detect airborne (volatile) odorants (Dulac and Torello, 2003). Odorants of heavier molecular weight (nonvolatile) are detected through the VS. Functionally, the division of labor between these systems has been an intense point of discussion for decades (Stephan et al., 1982; Frahm, 1985). Early insights into function of the vomeronasal organ (VNO) in rodents (Wysocki, 1979) have yielded a tendency to generalize that the VS detects pheromones while the MOS detects most other chemical signals. However, it is becoming clearer that in mammals some pheromones are easily detected by the MOS and that the VS is at least capable of detecting odorants that do not have pheromonal function (Wysocki and Preti, 2004, this issue). Early analyses of the VS debated the pheromonal versus nonpheromonal functions of this system in primates (Stephan et al., 1982), and it seems necessary to revisit this discussion based on the functional overlap of the MOS/VS in some other mammals. It is also critical to emphasize that although New World anthropoids apparently possess an intact VS (i.e., possess the receptor organ, vomeronasal nerves, and an accessory olfactory bulb), there is no convincing evidence whatsoever that it is functional for pheromone (or any odorant) detection (Barrett et al., 1990). In strepsirrhines, there is reason to believe the VS is critical for pheromonal communication (Aujard, 1997; Alport, 2004, this issue; Kay et al., 2004, this issue).
Anatomically, structural elements of both systems have played critical roles in the discussion of primate evolution and sensory specializations of extant primates. A number of authors have discussed size differences in the main olfactory bulb (MOB) between diurnal and nocturnal primates (Baron et al., 1983; Martin, 1990; Kay et al., 2004, this issue; Bush et al., 2004b, this issue). In this issue, Bush et al. (2004b), conclude that Parapithecus grangeri had intermediate retinal ganglion cell counts and olfactory bulb volume compared to extant strepsirrhines and anthropoids. Their findings may ultimately affect our understanding of sensory specializations that were present in stem anthropoids. In another study, Kay et al. (2004, this issue) conclude that the fossil platyrrhine Tremacebus harringtoni was not nocturnal, which narrows the possible dates for secondary evolution of nocturnality in ancestors of the extant owl monkey.
Broadly speaking, studies of primate olfactory bulb size illustrate some general trends in that visually adapted diurnal species have relatively smaller MOBs than nocturnal species. It may be worth considering that activity patterns offer only indirect correlates of MOB size. For instance, dietary specializations explain some variation in MOB volume in either diurnal or nocturnal species (Barton et al., 1995). It would be equally interesting to know whether varied patterns of social behavior (e.g., scent marking) (Epple et al., 1993; Irwin et al., 2004) relate strongly to MOB size. To date, behavioral correlates of the size of chemosensory structures have usually been discussed in relation to accessory olfactory bulb size (Stephan et al., 1982). There have been few explicit attempts to study social correlates of MOB size in primates.
Thus, a tendency to generalize about these parallel but anatomically distinct olfactory pathways, primarily based on knowledge about mammals with a well-developed VNO (e.g., rodents or opossums) (Halpern and Martínez-Marcos, 2003), obscures an integrated picture of the sensory systems. Recent attempts to understand a possible evolutionary trade-off between vision and olfaction have focused separately on the MOS (Rouquier et al., 2000; Gilad et al., 2004) and the VS (Liman and Innan, 2003; Zhang and Webb, 2003; Webb et al., 2004). Whereas these studies have important implications concerning the evolution of each system, it is difficult to understand the implications concerning particular functions (e.g., pheromonal communication) when it is not clear which olfactory system mediates that function in primates. There is clearly a need for more studies considering multiple permutations for how particular patterns of primate behavior may be mediated by neural structures.
The study by Alport (2004, this issue) is an important departure, examining whether intrasexual competition relates to MOB or neocortical volume in haplorhines. Studies that consider the roles of multiple neural pathways in mediating behavior are scarce (Barton et al., 1995; Alport, 2004, this issue), but may be the best route for dealing with the overlap in function of chemical senses. Regarding primates, this avenue may be especially important when considering that flavor is both gustatory and olfactory (Rolls, 2004, this issue). A similar combinatorial function has been suggested for the MOS and VS (Dennis et al., 2003).