Form

The Nocturnal Visual Predation Hypothesis (NVPH) argues that in the first modern primates, a shift to nocturnal visual predation on small invertebrates and vertebrates necessitated more anteriorly directed and medially approximated orbital apertures and eyeballs (Figure 6A) (Cartmill, 1970, 1972, 1974, 1992; also Collins, 1921). This increased orbital convergence in turn results in a larger binocular field for greater stereoscopic vision, as well as an exceptionally clear retinal image during nocturnal prey location and capture at short distances (Allman, 1977, 1982; Cartmill, 1970, 1972, 1974, 1992). The NVPH further explains the relatively larger orbits and grasping hands/feet possessing digits with nails as basal euprimate adaptations to nocturnality in an arboreal, terminal-branch milieu (Cartmill, 1970, 1972, 1974, 1992; Covert and Hamrick, 1993; Dagosto, 1988; Hamrick, 1998, 1999; Heesy and Ross, 2001; Kay and Cartmill, 1974, 1977; Kay and Kirk, 2000; Lemelin, 1999). In contrast, putative ancestors had the primitive mammalian condition of relatively small and less convergent orbits, larger olfactory complexes, digits with claws, and more terrestrial locomotor specializations (Cartmill, 1970, 1972, 1974, 1992; Kay and Cartmill, 1974, 1977; but see Bloch and Boyer, 2002; Bloch et al., this volume). Aside from alternative and less compelling claims that convergent orbits and grasping appendages are adaptations for nocturnal visual foraging on fruits and flowers in terminal branches (Crompton, 1995; Rasmussen, 1990; Sussman, 1991), the NVPH has become a well-accepted model of eupri-mate origins (Fleagle, 1999; Martin, 1990, 1993; Ravosa et al., 2000a).

The NVPH also addresses the correlated effects of changes in orbital form on the function of the circumorbital region. During molar chewing and bit-

Figure 6. Dorsal (A) and lateral (B) views of an adult greater galago skull (adapted from Ravosa et al., 2000a). Orbital convergence (A) refers to the extent the orbital margins face forward, such that orbits directed more anteriorly are convergent (arrow). This morphology is posited to facilitate binocular stereoscopic acuity and increased depth perception. Orbital frontation (B) refers to the degree of verticality of the margins, such that orbits more orthogonal to the cranial long axis are frontated (arrow). This condition appears linked primarily to greater basicranial flexion and ultimately increased levels of encephalization. Basal primates are derived relative to plesiadapi-forms and other sister taxa in exhibiting greater convergence and increased frontation.

Figure 6. Dorsal (A) and lateral (B) views of an adult greater galago skull (adapted from Ravosa et al., 2000a). Orbital convergence (A) refers to the extent the orbital margins face forward, such that orbits directed more anteriorly are convergent (arrow). This morphology is posited to facilitate binocular stereoscopic acuity and increased depth perception. Orbital frontation (B) refers to the degree of verticality of the margins, such that orbits more orthogonal to the cranial long axis are frontated (arrow). This condition appears linked primarily to greater basicranial flexion and ultimately increased levels of encephalization. Basal primates are derived relative to plesiadapi-forms and other sister taxa in exhibiting greater convergence and increased frontation.

ing, the lateral orbital margins on both sides of the face, thought to be pulled posteroinferiorly by the masseter and temporalis (Cartmill, 1970, 1972)—a loading pattern which is supported by the galago WS (but not BS) postorbital bar strain data (Figure 1B) (Ravosa et al., 2000a,b). In species with increased convergence, the orbital apertures are directed more out of the plane of the temporal fossa, and the above-circumorbital loading regime is posited to entail greater disruption of the orbital contents. Thus, the lateral orbital margins of taxa, like euprimates, are compressed more along the optical axis instead of along the orbital aperture as in more primitive mammals with lower convergence levels (Cartmill, 1970, 1972). It follows that to ensure a high degree of stereoscopic acuity in a nocturnal organism that hunts and forages while processing its prior meal,4 the postorbital bar of visual predators arguably functions to stiffen the lateral orbital margins and thus resist ocular deformation during mastication (Cartmill, 1970, 1972).

Though more vertical, frontated orbital apertures also deviate from the plane of the temporal fossa (Figure 6B), the role of orbital frontation has not figured into discussions on the origin of the primate postorbital bar (Cartmill, 1970, 1972). This dichotomy between the effects of convergence versus frontation on postorbital bar development and ocular movements is arguably unnecessary. Variation in one or both orbital parameters could influence postorbital bar formation. In fact, the visually oriented frugivore Caluromys differs from other didelphimorphs in exhibiting increased frontation (but not greater convergence - see in a later section), a relatively larger brain and larger postorbital processes of the frontal and jugal bones (Cartmill, 1970, 1972, 1974, 1992; Rasmussen, 1990).5 Due to both elevated convergence and frontation, the anthropoid postorbital septum is also posited to function in dampening ocular oscillations (Cartmill, 1980; Ross, 1995). In addition to higher convergence levels, basal primates were more encephalized and frontated than plesiadapiformes (Cartmill, 1992; Fleagle, 1999; Martin, 1990; Simons, 1962; Szalay and Delson, 1979).

To investigate the relationship between orbital orientation and the presence of a postorbital bar, three clades varying interspecifically in postorbital bar formation were examined (pteropodids, herpestids, felids - Noble et al., 2000; Ravosa et al., 2000a). To assess the link between increased orbital convergence and visual strategy, as well as phylogenetic and size-related patterns of orbital form in primate and nonprimate mammals, a series of adult interspecific analyses were performed (Ravosa and Savakova, 2004). As the presence of

4 One possible shortcoming of the NVPH is that it is unclear whether an organism would actively predate and/or forage while simultaneously chewing. If most animals are sedentary while eating, then why would a rigid postorbital bar be necessary for a high level of visual acuity (when predation is temporarily interrupted)? One related observation is that, unlike squirrels that return to the center of a tree when feeding, basal euprimate and nonprimate analogs tend to remain on terminal branches and thus apparently maintain elevated activity levels (cf. Cartmill, 1992).

5 In a didelphimorph marsupial sample with species means of 30-38 mm for the nasion-inion chord (n = 7 taxa, 68 adults), three sister taxa of the genus Caluromys (mean = 44.7°, range = 42.4-48.9°) are significantly more frontated than four species of the genera Philander, Chironectes, and Metachirus (mean = 32.2°, range = 25.3-37.7°) (Mann-Whitney U test, p = 0.034).

intrafamilial variation in activity cycle is vitally important for evaluating competing explanations for forward-facing orbits, phylogenetically restricted comparisons were performed in seven didelphimorphs (n = 68),6 11 procyonids (n = 88), 28 herpestids (n= 183), and five tupaiids (n = 21). To examine relative and absolute levels of orbital convergence in the earliest euprimates, four omomyids (n=8, nocturnal predators) and four adapids (n=12, diurnal foragers) were compared to functional analogs and sister taxa: 11 extant primate nocturnal predators (n = 48),7 31 felids (n = 208, nocturnal predators), 28 herpestids (n= 183, mostly diurnal predators), a dermopteran (n= 6, nocturnal foragers), five tupaiids (n = 21, mostly diurnal predators), 64 pteropodids (n = 277, nocturnal foragers), and two plesiadapiforms (n = 2, diurnal foragers) (Ewer, 1973; Fleagle, 1999; Martin, 1990, 1993; Nowak, 1999; Richard, 1985; Simons, 1962; Zeveloff, 2002). A benefit of this last, higher-level comparison over prior work (Ravosa et al., 2000a) is the inclusion of data for the most appropriate analogs based on body size, activity cycle, and feeding behavior for the first modern primates: living primate nocturnal predators.

The allometry of orbital orientation was further investigated for the postnatal ontogeny of six strepsirhines: Propithecus verreauxi (11 adults and 24 nonadults), Eulemur fulvus (10 adults and 27 nonadults), Hapalemurgriseus (11 adults and 20 nonadults), Otolemur crassicaudatus (11 adults and 21 nonadults), Nycticebus coucang (12 adults and 31 nonadults), and Perodicticus potto (12 adults and 34 nonadults) (Ravosa and Savakova, 2004). These primates were selected because they represent both extant strepsirrhine infraorders and most extant superfamilies, equal the interspecific range of variation in primate convergence values, and closely approximate the skull morphology of basal euprimates. In all taxa, at least five adults of each sex were examined.

Was this article helpful?

0 0

Post a comment