Visual System of the Only Nocturnal Anthropoid, Aotus: The Owl Monkey

Abstract

Diurnal haplorhines exhibit derived traits for high-acuity photopic vision, unique across mammals, and many other vertebrates. Yet, sometime in the mid-Miocene (12–15 MYA), the ancestor of owl monkeys shifted to a nocturnal activity pattern, which requires different visual morphology, including fundamental changes in retinal anatomy, that conflicts with the demands of a diurnal system. As one of only two night-active haplorhines, Aotus offers a unique opportunity to investigate how a visually oriented primate has adapted to low light environments. In this chapter, we synthesize data from anatomy, neuroscience, psychophysics, genetics, and behavioral ecology to review the key adaptations of the owl monkey visual system for dim light vision. First, we review Aotus evolutionary history and highlight the dramatic variation available in light environments at night. We next describe aspects of the visual system that allow nocturnal animals to experience “nighttime” differently than diurnally adapted humans. Finally, we situate Aotus within a broader comparative framework by contrasting their visual features with those observed in other primarily night-active primates (tarsiers, lemurs, and lorisiforms). Even compared to nocturnal strepsirrhines, owl monkeys exhibit a number of derived traits for high acuity vision in dim light. Moreover, although both owl monkeys and tarsiers transitioned to nocturnality from a diurnal haplorhine ancestor with high visual acuity, it appears that the two species followed very different paths in their evolution of dim light vision.

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Chapter 7
Visual System oftheOnly Nocturnal
Anthropoid, Aotus: TheOwl Monkey
CarrieC.Veilleux andChristopherP.Heesy
Abstract Diurnal haplorhines exhibit derived traits for high-acuity photopic vision,
unique across mammals, and many other vertebrates. Yet, sometime in the mid-
Miocene (12–15MYA), the ancestor of owl monkeys shifted to a nocturnal activity
pattern, which requires different visual morphology, including fundamental changes
in retinal anatomy, that conicts with the demands of a diurnal system. As one of
only two night-active haplorhines, Aotus offers a unique opportunity to investigate
how a visually oriented primate has adapted to low light environments. In this
chapter, we synthesize data from anatomy, neuroscience, psychophysics, genetics,
and behavioral ecology to review the key adaptations of the owl monkey visual
system for dim light vision. First, we review Aotus evolutionary history and highlight
the dramatic variation available in light environments at night. We next describe
aspects of the visual system that allow nocturnal animals to experience “nighttime”
differently than diurnally adapted humans. Finally, we situate Aotus within a broader
comparative framework by contrasting their visual features with those observed in
other primarily night-active primates (tarsiers, lemurs, and lorisiforms). Even
compared to nocturnal strepsirrhines, owl monkeys exhibit a number of derived
traits for high acuity vision in dim light. Moreover, although both owl monkeys and
tarsiers transitioned to nocturnality from a diurnal haplorhine ancestor with high
visual acuity, it appears that the two species followed very different paths in their
evolution of dim light vision.
C. C. Veilleux (*)
Department of Anatomy, College of Graduate Studies, Midwestern University,
Glendale, AZ, USA
e-mail: cveill@midwestern.edu
C. P. Heesy
Department of Anatomy, College of Graduate Studies, Midwestern University,
Glendale, AZ, USA
College of Veterinary Medicine, Midwestern University, Glendale, AZ, USA
© Eduardo Fernandez-Duque 2023
E. Fernandez-Duque (ed.), Owl Monkeys, Developments in Primatology:
Progress and Prospects, https://doi.org/10.1007/978-3-031-13555-2_7

204
7.1 Introduction
Primates display multiple visual features that distinguish them from other mammals
(Martin 1990). Anthropoid primates especially exhibit a suite of highly derived
morphological and neural adaptations for increased visual acuity and enhanced
color discrimination in bright light conditions (Ross 2000; Kirk and Kay 2004; Ross
and Kirk 2007; Jacobs 2008; Veilleux and Kirk 2014). Owl monkeys (Aotus) offer a
valuable counterexample to the primate and anthropoid trend, exhibiting a loss of
visual acuity and color discrimination associated with their transition to nocturnality
(Jacobs 1977b; Jacobs etal. 1996). While it has traditionally been assumed that
nocturnal mammals do not rely heavily on vision, relative to other senses, for
ecological tasks (e.g., Walls 1942, but also more recently Tan etal. 2005), a growing
consensus suggests that visual cues can be ecologically important for nocturnal
primates and other nocturnal vertebrates (Bicca-Marques and Garber 2004; Bearder
etal. 2006; Kelber and Roth 2006; Siemers etal. 2007; Piep et al. 2008; Valenta
etal. 2013; Veilleux et al. 2014). Owl monkeys provide a valuable comparative
model in visual neuroscience to contrast the data and models derived from the most
commonly used primate neuroscience model, diurnal macaques (e.g., Allman and
Kaas 1971; Kaas etal. 1972; O’Keefe et al. 1998; Xu et al. 2001; Ichida and
Casagrande 2002; Finlay etal. 2014). In this chapter, therefore, we synthesize and
review the key features of the owl monkey visual system benecial for dim light
environments and their associated visual behavior in order to place Aotus within a
broader comparative framework that considers other night-active primates such as
tarsiers, lemurs, and lorisiforms. Furthermore, we use these comparisons to highlight
limitations of relying on strict nocturnal/diurnal categorizations of diel activity for
considering the functioning of visual systems across a continuum of light
environments.
7.2 Haplorhine Evolutionary History andActivity Pattern:
Out intheLight andBack Again
7.2.1 Transition 1: Nocturnality toDiurnality
It is generally agreed that the earliest primates were likely nocturnal (Martin 1990;
Cartmill 1992; Sussman 1995; Heesy and Ross 2001; Ross etal. 2007; Heesy 2009;
Heesy and Hall 2010; Veilleux etal. 2013, but see Ni etal. 2004; Tan etal. 2005),
and therefore, the evolution of haplorhine primates has long been associated with a
presumed shift to a diurnal activity pattern (Ross 1996, 2000; Kirk and Kay 2004).
Indeed, the earliest stem haplorhine and anthropoid fossils from the early to middle
Eocene (e.g., haplorhine Archicebus, 55MYA; eosimiid anthropoids Bahinia and
Phenacopithecus, and late middle Eocene anthropoid Aseanpithecus, 40 MYA)
have relatively small orbits that are characteristic of extant diurnal anthropoids (Kay
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205
and Cartmill 1977;Heesy and Ross 2004; Beard and Wang 2004; Ni et al. 2013;
Jaeger etal. 2019). This presumed shift in activity pattern radically changed the
light environments encountered by these early haplorhines. In general, strictly
nocturnal and diurnal light environments impose conicting demands on animal
vision (Walls 1942; Hughes 1977; Warrant 2004; Land and Nilsson 2012). The
amount of light available constrains vision at night, typically resulting in selection
for adaptations that increase the sensitivity of the eye (Walls 1942; Lythgoe 1979;
Ali and Klyne 1985; Cronin etal. 2014). These traits, however, virtually always
come at the cost of ne detailed vision (e.g., visual acuity) and color discrimination,
as we discuss below.
With the shift to diurnal light environments, early haplorhines were freed from
the constraints of dim light on their visual systems. Selection for increased visual
acuity, possibly associated with visually guided faunivory (Ross 2000; Heesy and
Ross 2004; Kirk 2006a, Ross and Kirk 2007; Veilleux and Kirk 2014), led to the
evolution of several highly derived visual features, many of which are unique to
haplorhines across all mammals. Compared to both strepsirrhine primates and other
mammals, for example, diurnal haplorhines possess a postorbital septum, which
insulates the orbital contents from the actions of the masticatory muscles,
signicantly smaller corneas relative to eye size, short wavelength lters in the
retina (the macula lutea) and lens, and a retinal fovea composed exclusively of
cones (Ross 2000; Kirk 2004; Kirk and Kay 2004; Ross and Kirk 2007). These
anatomical features support high visual acuity; not surprisingly, diurnal haplorhines
possess signicantly higher acuity relative to eye size than strepsirrhines or other
mammals (Veilleux and Kirk 2014). Indeed, as a clade, only diurnal raptors exceed
diurnal haplorhines in acuity (Ross 2000; Kirk and Kay 2004; Caves etal. 2018;
Potier etal. 2020).
Moreover, all diurnal haplorhines have evolved derived color vision systems.
Howler monkeys (platyrrhine genus Alouatta) and all catarrhines exhibit routine
trichromatic color vision, wherein all females and all males have three types of
retinal cones and can distinguish colors along the blue-yellow and green-red
dimensions (reviewed in Jacobs 2008). Excluding Alouatta, all other diurnal
platyrrhines have polymorphic trichromacy, where allelic variation at the X-linked
M/LWS opsin gene causes heterozygous females to have three types of cones and
trichromatic color vision, while homozygous females and all males have the
ancestral mammal condition of dichromacy (equals to two cone types, blue-yellow
color discrimination). Among all the orders of placental mammals, trichromatic
color vision developed only in primates (Jacobs 2009).
7.2.2 Transition 2+: Diurnality toNocturnality
toCathemerality?
Today, only two extant clades of haplorhines diverge from this derived diurnal con-
dition: tarsiers and owl monkeys. It is generally accepted that both have secondarily
transitioned back to dim light visual environments from a diurnal haplorhine
7 Visual System oftheOnly Nocturnal Anthropoid, Aotus: TheOwl Monkey

206
ancestor (Ross 1996; Kay etal. 1997; Williams etal. 2010; Fleagle 2013). Fossil
evidence hints at a very long history of nocturnal vision in tarsiers; Tarsius eocae-
nus, the earliest known fossil tarsier (45MYA), already possessed hypertrophied
orbits likely indicative of dim light vision (Rossie etal. 2006). By comparison, the
transition to nocturnality among owl monkeys is relatively more recent. Although
evidence of platyrrhines dates from the latest Eocene (36MYA: Bond etal. 2015),
the earliest denitive owl monkey (Aotus dindensis) from La Venta, Colombia,
comes from the middle Miocene (12–15MYA) (Setoguchi and Rosenberger 1987).
Aotus dindensis has the relatively large orbits and characteristic dental features of
extant Aotus species (Setoguchi and Rosenberger 1987). While some scholars sug-
gest that the early Miocene (20MYA) Tremacebus harringtoni displayed nocturnal
traits (e.g., Rosenberger 1984), analyses of orbit and olfactory fossae sizes nd
them most similar to extant diurnal platyrrhines (Kay and Kirk 2000; Kay etal.
2004, although see Rosenberger 2023 this volume).
Although behavioral and experimental data have found that most Aotus species
and populations display strict nocturnality (Erkert 1976; Erkert and Gröber 1986;
Garcia and Braza 1987; Wright 1989; Fernandez-Duque et al. 2008; Khimji and
Donati 2014), at least one lineage has returned to some diurnal activity. Aotus azarai
azarai, from the dry gallery forests in the Gran Chaco of Argentina and Paraguay,
exhibits regular activity during the day and night (Wright 1989; Fernandez-Duque
2003; Fernandez-Duque and Erkert 2006; Fernandez-Duque et al. 2010).
Comparative studies indicate that cathemeral activity in this subtropical A. a. azarai
population may be associated with the pronounced seasonality of the Gran Chaco
region relative to other more tropical Aotus species (Fernandez-Duque etal. 2008;
Khimji and Donati 2014). The transition to cathemerality may have happened
relatively recently, possibly coinciding with the drying of the Gran Chaco region
~7000–9000years ago (Babb etal. 2011).
7.3 Light Environments andConstraints onOwl
Monkey Vision
The light intensities available by night and by day impose conicting constraints on
animal visual systems (Walls 1942; Hughes 1977; Lythgoe 1979; Martin 1990;
Warrant 2004; Land and Nilsson 2012). In order to see reliably in dim light,
nocturnal eyes must capture as many photons of light as possible. However, light
environments can vary dramatically in both the total number of photons (light
intensity) and the number of photons of different wavelengths (i.e., colors) available.
The differences in the intensity and color of light environments between daytime,
twilight, and nighttime have been well explored (Lythgoe 1979; Pariente 1980;
Johnsen et al. 2006). However, less well appreciated is the complexity of light
environments available within “nighttime” (Warrant 2004; Gaston 2019). In fact,
any nocturnal animal, including owl monkeys, will encounter dramatic variation in
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the intensity and spectral quality (color) of light over the lunar cycle and across a
single night as the moon travels across the sky. In general, starlight is richer in
longer (“redder”) wavelengths, while moonlight is similar in color to sunlight
(Pariente 1980; Johnsen 2012; Warrant and Johnsen 2013). In open areas, with the
moon directly overhead, full moonlight is 100-fold brighter than starlight (Johnsen
etal. 2006). Most owl monkeys (and other nocturnal primates), however, experience
these light environments in rainforests or dry deciduous forests, not open areas.
Within forests, lunar altitude/elevation—that is, the height of the moon in the sky—
and, to a lesser extent, the openness of the canopy also profoundly inuence
nocturnal light (Veilleux and Cummings 2012; Veilleux 2020). This leads to an
interesting effect where, for a given location in a forest, a quarter moon at maximum
altitude (i.e., directly overhead) can provide more light than a full moon at a lower
one (Veilleux 2020). A moonless starlit night in the open canopy of a dry deciduous
forest may also be paradoxically brighter than a moonlit night in a closed canopy
rainforest (Fig. 7.1a). The vertical location of the observer in the canopy (e.g.,
understory vs. emergent trees, terminal branches vs. trunk) further inuences light
intensity of a given light environment (Endler 1993; Dominy and Melin 2020).
Further, there is variation in nocturnal light intensity associated with changing
distance of the moon from the Earth and even between waxing and waning moons
(both considered “quarter” moon; reviewed in Dominy and Melin 2020). Moreover,
the spectral quality of light (as measured by the relative abundance of different
wavelengths) also varies in forestsat night with lunar altitude, lunar phase, and
canopy openness, although less dramatically than the variation observed in forests
during the day (Fig.7.1a, b, Endler 1993; Veilleux and Cummings 2012). At night,
both closed canopy and more open canopy forests are richest in middle wavelengths
(~560nm), but less open microhabitats are relatively more impoverished in shorter
wavelengths (~420–520nm, Veilleux and Cummings 2012). These differences in
the spectral quality of light between habitats and microhabitats likely affect how
well owl monkeys can detect different stimuli. Thus, over the course of a single
night, owl monkeys must navigate a complex and dynamic light environment as
they travel, avoid predators, and forage through the forest.
Moreover, given that all owl monkey species (both cathemeral and nocturnal) are
also active during sunrise/sunset and twilight (Garcia and Braza 1987; Wright 1989;
Fernandez-Duque 2003; Fernandez-Duque etal. 2008; Link etal. 2023 this volume),
it is important to note that light environments exhibit remarkable changes during
these relatively brief periods. Specically, light intensity can change by over 1000-
fold as the sun travels from 11.4° above the horizon to 10.6° below the horizon (late
nautical twilight) (Johnsen etal. 2006). Meanwhile, these twilight environments are
much richer in shorter wavelengths (blues/violets) and impoverished in longer ones
relative to light environments in forests at night (Endler 1993; Johnsen 2012; Melin
etal. 2012; Veilleux and Cummings 2012; Dominy and Melin 2020). Therefore, an
owl monkey beginning activity in twilight can experience over 10,000,000-fold
difference in light intensity in the course of a single night. Cathemeral populations
active during both night and the central part of the day experience an exponentially
higher range of light intensities (Johnsen etal. 2006).
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208
Fig. 7.1 Characteristics of forest light environments. (a) Light intensity (log-transformed total
nocturnal irradiance) in μmol m−2s−1nm−1 and (b) light spectral quality (normalized nocturnal
irradiance across wavelengths) measured across comparable lunar phases in a dry deciduous forest
during the dry season (Kirindy Mitea National Park) and a rainforest (Ranomafana National Park)
in Madagascar across comparable lunar phases. Spectra represent averages of multiple
measurements at different locations in each forest. See Veilleux and Cummings (2012) for details
on data collection. Light environments under gibbous moon (e.g., 75–91% full moon) and crescent
moon (7–14% full moon) were sampled at comparable lunar altitudes between forests. Comparative
study of light in diurnal forests indicate that light environments are shared across continents
(Endler 1993), so we would expect that these nocturnal environments are similar to those
experienced by owl monkeys. For comparable spectra of twilight environments, see Endler (1993)
and Melin etal. (2012), as well as the comprehensive review of “liminal light” by Dominy and
Melin (2020)
Like most other vertebrates, owl monkeys possess a retina composed of both rod
and cone photoreceptors (Wikler and Rakic 1990). Light environments are often
divided perceptually into three major categories based on photoreceptor function
(Fig. 7.2). Rods primarily function in scotopic (dim light) environments (often
dened as <0.005cdm−2), while cones primarily function in photopic (bright light)
environments (often dened as >5cdm−2; Kelber and Roth 2006). Rods and cones
can both function in mesopic environments, which comprise the range of light
intensities in between scotopic and photopic (Fig.7.2). In the context of animal
vision, starlight is scotopic, while moonlight and dim twilight are considered
mesopic (Kelber and Roth 2006, see Fig.7.2). It is important to note that these
categorizations presumably are based on the intensity of these illuminants in open
areas, not the dimmer light from the illuminants under the forest canopy. However,
evidence from comparative animal vision suggests that the light intensities
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Fig. 7.2 The typical dynamic luminance range of rod and cone functions for a normal human tri-
chromat. Luminance is displayed in candelas (cdm−2) for a typical white paper in unobstructed
outdoor light. Cones function over 1011 range of illumination and rods over a range of 108, which
together represents a trillion-fold functional range. High acuity and color discrimination are
optimal in the photopic (cone-dominated) range of visual function. Chromatically poor but higher
sensitivity visual function is part of the scotopic (rod-dominated) visual functional range. Both
rods and cones function in mesopic ranges, which are intermediate and transitional light
environments, such as dusk and dawn. (Derived from Soule (1968), Pokorny and Smith (1994),
and Purves and Lotto (2011))
comprising mesopic conditions may be subjective and differ between species.
Nocturnal geckos, for example, have pure-cone retinas and can make cone-based
color discriminations in dim moonlight conditions (0.002cdm−2) and possibly even
dimmer (Kelber and Roth 2006). Many nocturnal animals possess adaptations,
which increase the light gathering ability of the eye and the sensitivity of the retina
(see Sects. 7.4.2 and 7.4.3), lowering the light intensities at which cones can
function. Consequently, light environments that are scotopic for diurnal haplorhines
like humans may be mesopic for owl monkeys.
7.4 Owl Monkey Adaptations toDim Light Vision
Owl monkeys, like other nocturnal mammals, exhibit a number of adaptations to
increase photon capture in dim light. These adaptations include anatomical changes
to the size and shape of the eye, which increase the eye’s ability to collect light, as
well as to the retina and related microstructures to increase sensitivity at the retina.
Moreover, owl monkeys prefer activity in brighter nocturnal light environments
(e.g., Fernandez-Duque 2011), which also represents a behavioral adaptation to dim
light vision. In this section, we integrate anatomical, neuroscience, genomic, and
behavioral data to offer a brief primer on the primate visual system and then detail
how owl monkeys diverge from the basic haplorhine or mammal pattern.
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210
7.4.1 Adaptations: Eye Size andShape
Eye Size Owl monkeys are often discussed in the context of their extremely large
“hypertrophied” eyes (Walls 1942; Martin 1990; Kay and Kirk 2000). The transverse
diameter and axial length of the eye are dramatically larger in Aotus (and Tarsius)
compared to diurnal haplorhines of similar cranial size (Kirk 2006a). In general,
larger eyes are predicted to have greater sensitivity in dim light because they have
larger cornea sizes, which increases the amount of light admitted to the eye (Walls
1942; Hughes 1977). Larger eyes also, however, offer a benet to visual acuity by
spreading the visual image across a greater number of photoreceptors, thus “animals
that need both high resolution and high sensitivity have particularly large eyes”
(p. 106, Land and Nilsson 2012). The evolution of hypertrophied eyes in owl
monkeys and tarsiers has been traditionally linked to their secondary transition to
nocturnality and their lack of a tapetum lucidum, which is a reective layer behind
the retina that increases sensitivity in dim light (Martin 1990; Kirk and Kay 2004).
However, as we discuss below (Sect. 7.4.2.1), claims regarding the absence of the
tapetum in owl monkeys may be erroneous.
Eye Shape In addition to eye size, the shape of the eye varies in relation to differ-
ent light environments. Eye shape is typically quantied as the size of the cornea
relative to eye length (e.g., Kirk 2004; Veilleux and Lewis 2011). Across terrestrial
vertebrates, diurnally adapted eyes (including those of diurnal haplorhines) have
longer axial lengths relative to corneal diameter, while nocturnal eyes have larger
corneal diameters relative to axial lengths (Walls 1942; Hughes 1977; Ritland 1982;
Kirk 2006a, b; Ross etal. 2007; Land and Nilsson 2012). The longer eyes and
smaller corneas of diurnal taxa increase the focal length of the eye and the size and
clarity of the retinal image, which allows higher visual acuity (e.g., Walls 1942;
Hughes 1977; Land and Nilsson 2012). By contrast, the shorter eyes and larger
corneas of nocturnal taxa admit more light into the eye and form a smaller, but
brighter, image on the retina, supporting better visual sensitivity in dim light.
Consistent with this pattern, owl monkeys and tarsiers both have considerably larger
corneas relative to eye size than diurnal haplorhines (Kirk 2004).
In general, mammals reliably follow this pattern of eye shape variation in regard
to activity pattern and overall light environment (Kirk 2004, 2006b; Veilleux and
Lewis 2011). However, when compared more broadly with other vertebrates, most
mammals group with nocturnal birds and lizards in eye shape, regardless of activity
pattern (Ross etal. 2007; Hall etal. 2012), demonstrating that the activity pattern-
driven variation observed in mammals is still subsumed within a general “nocturnal
vertebrate” eye shape. This effect likely reects changes in eye shape that
occurredearly in mammalian evolution during the nocturnal bottleneck, as well as
the development of other sensory systems, such as hearing, that led to a decreased
reliance on vision (Heesy and Hall 2010; Hall etal. 2012). Only diurnal haplorhines
exhibit eye shapes that consistently group with diurnal birds and lizards (Ross etal.
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211
2007; Hall and Ross 2007; Hall etal. 2012). Assuming that the ancestral haplorhine
also exhibited the “diurnal vertebrate” eye shape, owl monkeys and tarsiers have
both re-evolved the general nocturnal vertebrate eye shape, plotting with other
mammals, nocturnal birds, and nocturnal lizards (Kirk 2006b; Ross etal. 2007; Hall
etal. 2012).
7.4.2 Adaptations: TheRetina andRelated Microstructures
oftheEye
Owl monkeys differ markedly from diurnal monkeys in many aspects of retinal
anatomy. This chapter is not meant to be a comprehensive review of primate retinae,
of which many are currently available (e.g., Grünert and Martin 2020). Instead, we
highlight the unique retinal morphology of Aotus in the contexts of nocturnal
adaptation and phylogenetic history. The eye itself is composed of concentric,
functionally unied layers of tissue, with the sclera the most external layer, a middle
vascular layer composed of the choroid, and an internal retinal layer. The retina,
which develops embryologically from the optic cup as an extension from the brain,
has an internal neural layer and an external nonneural, or pigmented layer, bounded
externally by the choroid. The neural retina contains rod and cone photoreceptor
cells facing away from the pathway of light and ve broad classes of neurons or
glia: horizontal, bipolar, amacrine, interplexiform, and retinal ganglion cells (e.g.,
Dowling 2012), that work together in various ways to rene information about the
image that is passed on to the brain through the optic nerve.
Information travels two ways in the retina—horizontally, within the retina itself,
and vertically, beginning with light capture in the layer of rods and cones and ending
by leaving the eye through the optic nerve. Like the eye as a whole, the vertebrate
retina contains concentric layers dened as “outer” (= closer to the sclera, sclerad)
or “inner” (= closer to the centrally located vitreous body, vitread). There are three
layers of cell bodies that communicate among themselves using the two plexiform
layers that lie between them (Fig.7.3). Closest to the sclera, just internal to the
pigment epithelium, lies the outer nuclear layer, sometimes called the layer of rods
and cones, which contain the cell bodies of the photoreceptors. Photoreceptor cells
communicate with each other and the cells of the inner nuclear layer via the outer
plexiform layer. The inner nuclear layer contains the horizontal, bipolar, amacrine,
and interplexiform neuronal cell bodies, and these cells communicate with each
other and the next layer of cells via the inner plexiform layer. Finally, and most
internally, all this information transmits to the retinal ganglion cells, the axons of
which comprise the optic nerve. The most important pathway for the vertical transfer
of information runs from photoreceptor cells to bipolar cells to ganglion cells, while
the other cells facilitate horizontal transfer of information. Looking at the proportion
of these cells to each other reveals an enormous amount of information about how
that animal utilizes their light environment. We rst summarize the distribution of
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Fig. 7.3 Layers of the retina. Light passes through multiple cell layers before reaching the photo-
sensitive segments of photoreceptors or the pigmented retinal epithelium. Rods (shaded) and cones
(unshaded) connect to bipolar cells in the outer plexiform layer, which includes lateral connections
via horizontal cells. In the inner plexiform layer,bipolar cells connectrods (shaded bipolar) and
cones (unshaded bipolars) verticallyto retinal ganglion cells, with additional lateral connections
via amacrine cells. Photoreceptor cell bodies are found in the outer nuclear layer and bipolar, hori-
zontal, and amacrine cell bodies are found in the inner nuclear layer. The ganglion cell bodies are
within the ganglion cell layer, the axons of which comprise the adjoining ganglion ber layer.
Ganglion cell axons leave the eye through the optic nerve on the way to the brain
several cell types and then in separate sections examine cone photoreceptor varia-
tion and functional implications of varying densities of cells.
7.4.2.1 Retinal Epithelium andTapetum
The retinal, or pigment, epithelium lies sclerad (i.e., closer to the sclera) to the distal
portions of the outer segments of the rod and cone photoreceptor cells along the
pathway of light. In photopic-adapted vertebrates, the retinal epithelium is deeply
pigmented, containing melanocytes that, analogous to the matte black coatings
inside lm cameras, absorb excess light and glare. By contrast, dim-light-adapted
vertebrates often have a modied unpigmented epithelium that allows light to pass
through (Nicol 1981). In these scotopic-adapted taxa, the unpigmented epithelium
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pairs with the presence of a tapetum lucidum, a specialized reective layer found
sclerad to the retina that reects light back through the photoreceptor layer, thereby
providing additional chances for photon capture by photoreceptors (Pirie 1959,
1966). Vertebrate tapeta can vary in size, shape, and location within the eye but are
most often found in animals inhabiting dim or spectrally restricted light environments
(Walls 1942; Nicol 1981; Ali and Klyne 1985). Tapeta are typically divided into two
main types based on their cellular composition: (1) a tapetum cellulosum in which
reective cells stack in layers or (2) a tapetum brosum in which densely packed
collagen brils form the reective component (Nicol 1981; Ollivier etal. 2004).
Uniquely across vertebrates, strepsirrhine primates possess a tapetum cellulosum
composed of crystalline riboavin (Pirie 1959, 1966). Electrophysiological studies
in Otolemur crassicaudatus support the hypothesis that tapetal uorescence
contributes to increased visual sensitivity (Dartnall etal. 1965). In other non-primate
mammals with a tapetum cellulosum, such as carnivorans or the marsupial Didelphis,
the tapetum variably includes crystalline forms of zinc-cysteine, lipid forms of
cholesterol, or, in the paca, sulfur (Pirie 1966; Braekevelt 1993). Most cetartiodactyla
(except porcines) possess a tapetum brosum (Nicol 1981; Ollivier etal. 2004).
While phylogenetically unclear whether a riboavin-based tapetum cellulosum
evolved in the earliest primates or in ancestral strepsirrhines, the haplorhines
ancestral to both tarsiers and owl monkeys are believed to have lacked it (Martin
1990; Ross 2000; Martin and Ross 2005). Tapeta functionally increase sensitivity
but at the expense of resolution because both the spherical shape of the eye and the
varying refractive indices of the retinal layers and the tapetum would partially
scatter the reected light (Rodieck 1988; Braekevelt 1993). Tapetal optical glare
and blur would degrade the high visual resolution made possible by the cones
concentrated within and around the fovea of haplorhines, especially in photopic
conditions (e.g., Rodieck 1998). Although some scholars describe Aotus as lacking
a tapetum lucidum, Rodieck (1988) describes the presence of a well-dened tapetum
brosum in these animals (see also Rochon-Duvigneaud 1943). Rodieck (1988)
specically describes (unfortunately without accompanying histological sections)
densely concentrated collagenous bers of the owl monkey tapetum located directly
behind an unpigmented region of retinal epithelium. Jones (1965) also reported a
lightly pigmented retinal epithelial layer in Aotus trivirgatus. Gordon Walls reported
a tapetum brosum in Aotus, although later thought he had erred (1942, 1953). On
the other hand, the classic funduscopic studies conducted by Wolin and Massopust
(1967) found the highly reective fundus of Aotus problematic for imaging vascular
patterns and assumed the presence of a tapetum was the confounding morphological
factor. The presence of a tapetum brosum is consistent with descriptions of brilliant
eyeshine in wild owl monkeys (Walls 1942; Osorio et al. 2005). Additionally, a
region of modied unpigmented retinal epithelium adjacent to the tapetum (as
described in owl monkeys by Rohen and Castenholz 1967 and Rodieck 1988) is
typically present among vertebrates possessing tapeta. The presence and novel form
(for primates) of a tapetum brosum and modied retinal epithelial layer are, if
corroborated, derived adaptations of owl monkeys for enhanced sensitivity in
scotopic and mesopic light environments.
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7.4.2.2 Photoreceptors
Vertebrates possess two types of light-sensitive photoreceptor cells in their retinae:
rods and cones. Rods function maximally in scotopic conditions, whereas cones
function maximally in photopic conditions (Walls 1942). Photoreceptors encode the
light presented to the retina as a function of intensity varying with three factors:
position on the retina, wavelength, and time (Nassi and Calloway 2009). Like many
mammals, primates have far more rod than cone photoreceptors. Primates also vary
in the wavelength sensitivities expressed in their cones. While early reports on the
Aotus retina incorrectly described an all-rod photoreceptor complement (Woollard
1927; Detwiler 1941; Walls 1942), subsequent work identied cone photoreceptors
as well (Wikler and Rakic 1990).
Cone Opsins The visual pigments within rods and cones are G-protein-coupled
receptors, composed of a seven-transmembrane protein (opsin) and an 11-cis-retinal
chromophore located in the outer segments of the photoreceptor (Palczewski 2006).
The protein is called rhodopsin in rods and cone opsin in cones. The peak spectral
absorption of the photoreceptor (λmax) is determined by the amino acid sequence of
opsin genes, such that variation within an opsin gene changes the spectral sensitivity
of the photoreceptor (Hunt etal. 2009). While most placental mammals are limited
to one type of rod and two types of cone receptors (short-wavelength-sensitive SWS
cones, medium/long-wavelength-sensitive M/LWS cones), early platyrrhines were
likely characterized by polymorphic trichromacy, wherein allelic variation at the
X-linked M/LWS opsin gene results in the expression of both MWS and LWS cones
(see Jacobs 2008, 2009 for reviews of the evolution of primate and mammal color
vision).
Multiple opsin losses mark the visual evolution of owl monkeys relative to other
platyrrhines. First, in contrast to all diurnal platyrrhines, all Aotus individuals thus
far examined (across multiple species) have only one M/LWS cone type and are
monoallelic at the M/LWS opsin gene (Jacobs etal. 1993; Mundy etal. 2016). Thus,
the X-linked polymorphism maintaining trichromacy in other platyrrhines was
likely lost at some point early in owl monkey evolutionary history. The λmax of this
single M/LWS cone type is estimated at ~543nm using electroretinogram (ERG)
icker photometry methods in living animals (Jacobs etal. 1993) and ~539 nm
using visual pigment reconstitution methods (Hiramatsu etal. 2004). Second, early
owl monkeys also likely lost the blue-sensitive SWS cone (Levenson etal. 2007).
Immunohistochemistry initially demonstrated the absence of SWS cones in the owl
monkey retina (Wikler and Rakic 1990). Subsequent work found no evidence of
SWS cone contribution to vision using ERG in living animals (Jacobs etal. 1993)
and identied pseudogenization of the SWS1 opsin gene due to the accumulation of
deleterious mutations (Jacobs etal. 1996). At least one loss-of-function mutation in
the SWS1 opsin gene is shared across members of the northern and southern owl
monkey species groups (A. trivirgatus vs. A. azarai and A. nancymaae, respectively;
Fernandez-Duque etal. 2023 this volume), indicating that SWS1 was pseudogenized
prior to the divergence of the two groups (Levenson etal. 2007). As a result of these
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losses, all owl monkeys are cone monochromats and lack color vision in photopic
conditions (Jacobs etal. 1993), although there is a possibility of rod/cone color
vision in mesopic light (see below).
Loss of cone types as seen in owl monkeys has been linked with a nocturnal
activity pattern. All mammals, for example, lost two cone types relative to other
vertebrates during a nocturnal period in early mammal evolutionary history (Hunt
etal. 2009; Jacobs 2009; Heesy and Hall 2010). SWS cone loss, in particular, is
fairly common among nocturnal taxa across mammals (Peichl 2005; Jacobs 2013).
Presumably, the dimmer light environments available at night lead to reduced color
discrimination ability due to lower photon counts, and perhaps an increased
emphasis on luminance cues rather than chromatic cues for visual detection (Jacobs
2013; Moritz 2015; Veilleux 2020). Cone loss could be the result of a relaxation of
functional constraint on the opsin genes, leading to the accumulation of deleterious
mutations. Alternatively, it could represent an adaptive loss to eliminate the
metabolically expensive neural architecture needed to process color signals (Jacobs
2013) and instead emphasize luminance vision. However, many other nocturnal
mammalian taxa maintain SWS cone function (Veilleux and Cummings 2012;
Veilleux etal. 2013), indicating that nocturnality is necessary, but not sufcient, to
explain opsin loss in Aotus. The discovery of owl monkey SWS cone loss, the rst
such discovery among nocturnal mammals (Wikler and Rakic 1990; Jacobs etal.
1993, 1996; Jacobs 2013), sparked fascinating research that uncovered dozens of
species with SWS cone loss across multiple orders and stimulated exciting new
research questions regarding factors leading to SWS cone loss and retention in
nocturnal mammals (e.g., Tan etal. 2005; Perry etal. 2007; Zhao etal. 2009; Melin
etal. 2012; Veilleux etal. 2013; Melin etal. 2016; Moritz etal. 2017).
Interestingly, owl monkeys are unique across vertebrates in having evolved extra
copies of the M/LWS gene on the Y-chromosome (Kawamura et al. 2002; Nagao
etal. 2005; Jacobs 2007). This likely occurred through a duplication and translocation
event of the M/LWS gene from the X chromosome to the Y chromosome in the
ancestor of extant owl monkeys (Kawamura etal. 2002; Nagao etal. 2005). The
structure, number, and evolutionary history of these copies appear to vary between
northern and southern Aotus species groups. Nagao et al. (2005) found that in
A. lemurinus griseimembra (a member of the northern group), the M/LWS gene on
the Y-chromosome is intact and has been evolving in sync with the X-linked gene
under functional constraint. By contrast, while the molecular evidence implies that
the X- and Y-linked opsin genes were once evolving in sync in the southern group,
a fusion event between the Y-chromosome and an autosome in the ancestor of the
southern group may have led to a relaxation of selection on the Y-linked opsin genes
(Nagao et al. 2005). Consequently, the multiple copies of M/LWS on the Y
chromosome of A. azarai boliviensis are pseudogenized (i.e., lost function). It is
unknown what functional impact an intact Y-linked M/LWS opsin gene has for
members of the northern group, although it seems as though it would currently be
very limited. The sequence is identical to the X-linked gene, so if it is expressed in
male owl monkey cones, it would not lead to differences in color vision (Jacobs
2007). This situation does set up a very interesting scenario in the event of a future
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216
mutation at one of the spectral tuning sites in the Y-linked M/LWS opsin gene,
however. In such a hypothetical scenario, owl monkey males would exhibit more
rened color vision than females—a contrast to the female trichromacy in other
platyrrhines.
Rod Nuclear Architecture The structure of the rod photoreceptors reveals another
area of potential adaptation to dim light vision. The rods of most animals (including
diurnal mammals) exhibit a “conventional” nuclear architecture, with euchromatin
(i.e., loosely packed chromatin involved in transcription) restricted to the nuclear
interior and heterochromatin (i.e., tightly packed chromatin) located at the nuclear
periphery (Solovei etal. 2009). Most animals commonly display this architectural
patterning of the nucleus across their cells (Feodorova et al. 2020). Nocturnal
mammals, however, have uniquely evolved an “inverted” architecture in their rods,
with heterochromatin located in the center of the nucleus (Solovei etal. 2009; Joffe
etal. 2014). The centrally located heterochromatin acts as a “microlens,” channeling
light efciently to the photoreceptive rod outer segments, thereby reducing light
scatter and increasing the light capturing ability of the cell (Solovei etal. 2009;
Feodorova et al. 2020). This inverted architecture is thought to be a derived
adaptation developed during early mammalian evolution before the divergence of
placental and marsupial mammals, when most mammals were likely nocturnal
(Heesy and Hall 2010), with subsequent reacquisitions of the conventional pattern
in diurnal mammal lineages (Solovei etal. 2009; Feodorova etal. 2020). Diurnal
platyrrhines (and catarrhines) all exhibit the conventional pattern of rod nuclear
architecture; however, the rod nuclear architecture of owl monkeys is more
transitional (Joffe etal. 2014). While Aotus rod nuclei possess many features of the
diurnal conventional architecture (reective of its secondary transition to
nocturnality), they also possess a spherical block of heterochromatin in the center of
the nucleus that likely acts as a lens to increase light transmission, similar to the
inverted architecture of other nocturnal mammals (Joffe etal. 2014). This spherical
block of heterochromatin in owl monkeys is made up of a large segment of tandemly
repeating DNA (a megasatellite) named OwlRep (Koga etal. 2017; Nishihara etal.
2018). The OwlRep megasatellite is unique to Aotus and is found in both northern
and southern species groups (Nishihara etal. 2018). Thus, with the transition to
nocturnality early in owl monkey evolution, there was likely selective pressure to
re-evolve a centrally located block of heterochromatin to increase rod sensitivity in
dim light environments.
7.4.2.3 Retinal Topography andPhotoreceptor Densities
Beyond the optical properties inherent to eye size, the sensitivity and acuity of the
eye both relate to the presence, density, and distributions of retinal cells. Light,
combined with the physical topography of the animal’s environment, provides the
most important selective pressures on vertebrate retinal morphology to emphasize
either resolution or sensitivity (Hughes 1977; Peichl 2005; Land and Nilsson 2012;
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217
Moore etal. 2017). Many vertebrates exhibit a specialized portion of the retina that
represents the most commonly viewed part of the visual eld; this “area centralis”
routinely matches the shape of an animal’s visual object of interest. For example,
animals that keep their gaze on the horizon have a long, at area centralis in the
portion of the retina that is faced toward the horizon (Moore etal. 2017). Among
primates, the area centralis is located in the region of the temporal retina coinciding
with the visual axis with the highest density of photoreceptors, as well as bipolar
and retinal ganglion cells. In diurnal primates, the area centralis contains tightly
packed, small-diameter photoreceptors and a near one-to-one-to-one ratio of
photoreceptors to bipolar to retinal ganglion cells, resulting in the highest densities
of all of these cells and an area of high visual acuity (Rohen and Castenholz 1967;
Rodieck 1988, 1998). Unique among mammals, haplorhines possess an avascular
depression within the area centralis known as a fovea, created by the centrifugal
displacement of the retinal layers found vitread (i.e., toward the vitreous body) to
the outer nuclear layer where the photoreceptors reside (Polyak 1941, 1957; Walls
1942; Ross 2004). Scholars have debated functional hypotheses for the presence of
foveae in vertebrates for years (see Moore etal. 2017). The displacement of retinal
components away from the area centralis strongly associates with higher acuity in
vertebrates, since foveae give the photoreceptors a chance to capture light without
requiring the photons to penetrate all the layers of the retina in the unusual
“backward” morphology of the vertebrate retina with photoreceptors that face away
from light (Fig.7.3).
Owl monkeys have an area centralis with a higher density of retinal ganglion
cells, including the midget bipolar cells associated with higher acuity (Jones 1965;
Ogden 1974, 1975, 1983; Jacobs 1981). The routine presence of foveae, on the other
hand, is uncertain; foveae have been reported in Aotus as either variably, slightly,
and partially or fully present (Walls 1953; Wolin and Massopust 1967; Ogden 1974,
1975; Provis etal. 1998; Silveira 2004; Finlay et al. 2005). This wide range of
reported variation is likely largely due to variable methodological approaches1 and/
or variation among individuals, populations, species, or genera. Further, the central
displacement of retinal ganglion cells that typify haplorhine fovea has been reported
as “negligible” in Aotus (Jones 1965; Ogden 1974) and was not apparent in the
study conducted by Yamada etal. (2001). At present, it cannot be said for certain
how variable the fovea is in owl monkeys, nor how this variation relates to a
nocturnal lifestyle. However, foveae are rarely present in nocturnal animals, where
the animal cannot collect enough light to fuel increased visual acuity (Ross 2000);
tarsiers represent an interesting exception to this pattern (see Sect. 7.5.2).
Aotus has a very large total retinal area, as expected for its large eye size (Silveira
2004; Silveira etal. 2005; Finlay etal. 2005; Dyer etal. 2009). Owl monkeys also
have an extraordinarily large absolute number of rods per retina, with reports of
over 140million in A. azarai, the largest known complement of rod photoreceptors
1 For example, sample sizes and methods vary across studies, including the use of different histo-
logical techniques (e.g., different types of stains, such as the more modern targeted use of immu-
nohistochemistry), or ophthalmoscopic imaging.
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218
for its brain size among primates (Finlay etal. 2005; Dyer etal. 2009). The increase
in rods has come only partly at the expense of cone photoreceptors in Aotus (Finlay
etal. 2005). The distributions of photoreceptors in Aotus differ from other primates
(Fig.7.4), with a high concentration of rods within the central retina as well as
peripherally, whereas diurnal primates pack their area with cones. Both rods and
cones are found within the central retina, although rod:cone ratio in owl monkeys
varies between studies. While early work by Ogden (1975) found a ratio of 50:1in
the central and peripheral retina, later work (Wikler and Rakic 1990; Yamada etal.
2001) found lower rod:cone ratios in the central retina (14:1 or 24:1) and higher
ratios in the periphery (93:1 or 40:1). Some of this variation between studies is
likely due to methodological differences (e.g., anatomical preparation, sampling
interval calculations: Yamada et al. 2001). Yet, regardless of this variation, the
arrangement of photoreceptors in owl monkeys differs dramatically from the diurnal
pattern (Fig.7.4). Diurnal haplorhines exhibit a large peak number of cones and an
absence of rods in the central retina, with rods at higher densities only found in the
peripheral retina outside the area centralis (Yamada etal. 2001; Finlay etal. 2008).
7.4.2.4 Other Neural Cells intheRetina
Photoreceptors relay signals through bipolar cells to the cell contacts of the inner
plexiform layer. Processes of horizontal cells contact the photoreceptor-bipolar
synaptic sites and modify the spatial differences in light and dark intensity between
adjacent clusters of photoreceptors received by bipolar cells, which essentially acts
to enhance contrast discrimination (Rodieck 1998; Masland 2001).
Horizontal Cells Horizontal cells contact multiple neighboring photoreceptors
and thereby begin the formation of the center-surround receptive elds presented to
ganglion cells that make opponent stimulus weighted comparisons of input among
neighboring clusters of photoreceptors (Masland 2001). Anthropoids have either
two or three morphological classes of horizontal cells: H1, H2, and H3 (Polyak
1941; Krebs and Krebs 1991; Dacey 1999; Dacey etal. 1996; Silveira 2004; Silveira
etal. 2005). H2 horizontal cells exclusively contact cones, whereas both H1 and H3
cells can have both rod and cone contacts. H1 horizontal cells are also known to
preferentially contact both MWS and LWS cones over SWS cones (e.g., Ahnelt and
Kolb 2000). H2 cells notably demonstrate large responses to stimuli for SWS cones
when compared to longer wavelength stimuli (Dacey etal. 1996). Among the major
differences between Aotus and diurnal anthropoids, especially when compared to
Cebus, is the rarity or absence of the H2 horizontal cell class in the former (Dos
Santos etal. 2005; Silveira 2004). The loss of the SWS cone that occurred during
the owl monkey transition to nocturnality likely explains this lack of H2 horizontal
cells. Owl monkey H1 horizontal cells display an increased size with larger dendritic
trees when compared to Cebus for most of the retina with the exception of the far
periphery (Dos Santos et al. 2005). Larger dendritic eld sizes may reect the
relatively lower cone density in Aotus, resulting in an increase in size to maintain a
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Fig. 7.4 Rod and cone densities peak in the foveal region of Aotus, which is exclusively populated
by cones in diurnal haplorhines. Eccentricity on the x-axis refers to the distance in mm from the
foveal region (in Aotus) or fovea (in Cebus) across the retina. Positive and negative values represent
nasal and temporal eccentricities, respectively. Aotus has higher rod and lower cone densities at all
eccentricities across the retina than in a typical diurnal platyrrhine, Cebus (Sapajus). (Adapted and
reprinted from Yamada etal. (2001), with permission from Elsevier)
functional equivalence in the number of cones contacting each horizontal cell (dos
Santos etal. 2005).
Bipolar Cells Bipolar cells of many different morphologies contribute up to 20
visual pathways (Boycott and Wässle 1991; Rodieck 1998; Dacey 2004; Euler etal.
2014), which differ in the parsed form of visual information each carries as well as
the level of illumination required for their activation. In primates, just as in non-
primate mammals, there is only one known rod-specic bipolar neuron, whereas
many cone-contacting bipolars have been identied (Rodieck 1988, 1998, Daw
etal. 1990,reviewed by Grünert and Martin 2020). Owl monkeys have an absolutely
large number of bipolar cells, reecting the large number of rods within the retina
(Lameirão etal. 2009). Their bipolar cell densities are somewhat unusual with a
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220
“ringlike” peak of rod bipolar cells about 5° from the foveal position (Lameirão
etal. 2009). Ogden (1974) reported midget bipolar cells within their area centralis
typically associated with low retinal summation but, unlike diurnal anthropoids,
found these cells utilize dendritic arborizations with two cones. This type of two
cone-to-midget bipolar relationships is only seen in peripheral retinae of diurnal
anthropoids (Ogden 1974).
Nevertheless, in owl monkeys, as in other typical nocturnal mammals, multiple
rod photoreceptors converge on relatively few rod bipolar cells with greater
eccentricities from the area centralis (Rohen and Castenholz 1967; Peichl 2005).
This rod signal convergence, known as retinal summation, increases the visual
sensitivity because hyperpolarization of any rod in the array will signal to the bipolar
cell. However, this increased sensitivity comes at the expense of visual resolution,
because that same array of rods perceives a larger visual angle. In other words,
small or multiple visual stimuli within that region cannot be distinguished apart.
Therefore, the increase of rod density and decrease in ganglion cell density with
greater retinal eccentricity characteristic of owl monkeys substantially increase
visual sensitivity (Finlay etal. 2008; Lameirão etal. 2009).
M, P, and K Pathways Current, and likely conservative, estimates of the number
of retinal ganglion cell (RGC) types in primates reveal 22 to 30 types based on
morphological (size and shape), neurophysiological, neurochemical, or connectivity
criteria (Rodieck 1998; Kaplan 2014). It is conceptually useful to think of retinal
ganglion cells as lters that, because of their functional and physiological variation,
encode in parallel highly specic properties of an image and then project these
encoded features to functionally differentiated visual centers in the brain (Boycott
and Wässle 1999). Yet, despite RGC diversity, roughly 90% of retinal ganglion cells
group into three general functional categories, at least in macaques (Nassi and
Calloway 2009). Contemporary convention for vision research discusses these three
general RGC categories as contributing to three parallel visual streams known in
primates (Casagrande 1994; Casagrande and Xu 2004; Casagrande et al. 2009;
reviewed in Baldwin and Bourne 2017) from the retina through the thalamus to the
visual cortex (i.e., the retinogeniculostriate pathway). Magnocellular (M, meaning
large-celled) retinal ganglion cells (often referred to as parasol cells) have large cell
bodies and dendritic processes with distributed connectivity, lower responsiveness
to spatial frequencies, but higher responsiveness to both temporal frequencies and
higher contrast sensitivities (Casagrande etal. 2009). Magnocellular cells form the
luminance channel of visual information and do not contribute to color discrimination
because of summing of red and green signaling. This pathway attunes to luminance
changes, often described as functioning to detect movement and object location in
space (Kremers etal. 1999).
Parvocellular (P, meaning small-celled) ganglion cells have much smaller cell
bodies and dendritic distributions with comparatively higher responsiveness to
spatial frequencies but lower temporal resolution and contrast sensitivity. Primates
appear to be unique in exhibiting small specialized parvocellular cells, called midget
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ganglion cells, in the foveal and parafoveal regions (Polyak 1941, 1957). These
midget ganglion cells are characterized by a near one-to-one cone-bipolar-midget
ganglion cell pathway, likely for high resolution (Polyak 1941, 1957; Walls 1942).
Parvocellular cells also contribute to chromatic/color opponency, a key component
to the preprocessing of color information, whereas magnocellular cells do not.
Consistent with their role in detecting movement, magnocellular cells also display
much higher conduction velocities than parvocellular cells due in part to larger
axonal diameters, which act to decrease the signal delay from the peripheral retina.
Lastly, the comparatively heterogeneous koniocellular (K, referring to tiny or
“dustlike”) ganglion cells are often classied as bistratied based on the anatomy of
their dendritic distribution, with functional properties that vary not only among
species but also occasionally between interlaminar regions of the same species
(Casagrande and Xu 2004). K cell regions also contribute to blue-yellow signaling
along other pathways (Dacey and Lee 1994; Hendry and Casagrande 1996; Martin
etal. 1997; Hendry and Reid 2000; Martin and Grünert 2013).
While the P pathway is especially well developed in anthropoids, likely associ-
ated with their high visual acuity and color discrimination (Kirk and Kay 2004; Kirk
2006a, b), owl monkeys appear to diverge from the diurnal anthropoid pattern.
Aotus azarai and A. infulatus had higher proportions of M to P cells than Cebus
(Sapajus) apella (Yamada et al. 2001), reecting an emphasis on increased
sensitivity within a dim light environment. Aotus has higher rod signal convergence
but similar cone convergence to both M and P cells compared to other anthropoids
(Yamada etal. 2001). Yamada and colleagues interpreted this nding as indicating
that: “...the owl monkey retina has undergone changes compatible with a more
nocturnal lifestyle, but kept a cone to ganglion cell relation similar to that found in
diurnal primates” (p119). Higher rod convergence on both M and P retinal ganglion
cells likely increases the luminance (i.e., perceived brightness) sensitivity of both
pathways (Yamada et al. 2001; Silveira 2004). The range of the rod signal
contributions to both M and P pathways in owl monkeys also extends to much
higher retinal light levels than typically anticipated by rod physiology and at light
intensity levels where Cebus (Sapajus) ganglion cell responses are dominated by
cones (Silveira etal. 2004). The regular spacing of cones within the area centralis
(approximately 10μm apart, Ogden 1975) is too coarse to account for behaviorally
measured visual acuity estimates (Jacobs 1977b). It is likely that the P ganglion cell
complement within the area centralis is responsible for owl monkey behavioral
acuity estimates not just because of the inter-cone spacing but also because the M
ganglion cells lack the one-to-one connections of photoreceptors to bipolars to
RGCs (Yamada etal. 2001). Thus, taken together, the extended light intensity range,
luminance sensitivity, and P ganglion density suggest that rod signals are contributing
to resolution functions at mesopic light levels in owl monkeys.
Additionally, owl monkeys appear to lack the small bistratied ganglion cells
associated with the blue-yellow color discrimination channel through the
koniocellular pathway (Yamada et al. 2001; Dos Santos et al. 2005), which are
involved in color vision in dichromatic and trichromatic platyrrhines (e.g., Martin
etal. 1997; Martin and Grünert 2013). This absence in Aotus may be linked to SWS
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222
cone loss and the associated loss of the blue-yellow color channel. Given that these
small bistratied ganglion cells contribute substantial input to the koniocellular
pathway in other platyrrhines (Martin etal. 1997; Martin and Grünert 2013), it is
especially interesting that the koniocellular receptive layer in the lateral geniculate
nucleus is expanded in this genus relative to other anthropoids. Therefore, which
retinal ganglion cells contribute the majority of input to the koniocellular pathway
in owl monkeys remains unclear.
7.4.3 Adaptations: Retinogeniculostriate Pathway
Optic Chiasm Retinal ganglion cells (RGCs), the projection neurons of the verte-
brate retina, deliver axons to the lateral geniculate nucleus of the thalamus. RGC
axons travel from the eyes in the optic nerves, which meet at the midline optic chi-
asm. The optic chiasm allows for the decussation (crossing over) of some propor-
tion of RGC axons to the contralateral side. Generally, in primates and carnivorans,
the axons from the temporal retinal region continue dorsally along the ipsilateral
side, whereas those from the nasal retina cross via the chiasm to continue within the
contralateral optic tract. The organization and pathway of optic nerve bers at the
optic chiasm is itself hypothesized to be a mammalian adaptation for nocturnality
(Heesy and Hall 2010). In non-mammal vertebrates, 100% of optic nerve bers
decussate to the contralateral side at the optic chiasm (Butler and Hodos 2005). In
all mammals, however, some portion of the bers continue dorsally along the ipsi-
lateral side, which provides the basis of binocular vision and offers an advantage in
dim light vision, as it gives both eyes the chance to capture a given photon of light.
In mammals, the proportion of ipsilateral versus contralateral RGC axons varies in
rough proportion to the extent of the binocular visual eld, with primates displaying
the highest contralateral decussation of RGC axons and highest binocular eld over-
lap among mammals with 50% of the bers crossing over (Walls 1942; Heesy etal.
2011). The optic tracts continue dorsally and deliver the majority of the RGC axons
to either the lateral geniculate nucleus (LGN) of the dorsal thalamus or the superior
colliculus, part of the midbrain (Kaas etal. 1972). This latter structure coordinates
visually based reexes and visually guided behavior, and the bilateral, binocular
visual eld representation within it that is found in primates may be unique among
mammals (Kaas and Preuss 1993; Preuss 2009). The superior colliculus also con-
tributes a substantial volume of feedback axons to the LGN (Casagrande and Royal
2004; Sherman and Guillery 2006, 2013). In primates, approximately 80% of RGC
axons project to the lateral geniculate nucleus (Kaas et al. 1972). However, in
rodents and lagomorphs, a far larger proportion of RGC axons project to the supe-
rior colliculus than to the LGN, possibly reecting the primitive mammalian condi-
tion (Baldwin and Bourne 2017).
Lateral Geniculate Nucleus The walnut-shaped right and left thalamus, conglom-
erations of nuclei found deep to the cerebral cortex, provide the key gateway for
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223
sensory information entering, and motor commands exiting, the cerebral cortex
(Jones 2007; Sherman and Guillery 2006, 2013). The dorsal LGN comprises the
thalamic relay projecting visual information to the cortex, specically to Area V1
(striate or primary visual cortex). Lateral geniculate nuclei organize information
retinotopically, meaning they maintain the retinal topography of the ganglion cells
within the layers of the LGN. These layers divide and segregate into lamina or
layers of distinctly staining cell bodies (Jones 2007). The retinotopic organization
of each layer precisely registers across layers, so the position of a visual stimulus
within one LGN layer is identical in the adjacent LGN layers (Kaas etal. 1978;
Kaas and Huerta 1988; Kremers etal. 2005). In the non-primate mammals for which
the most data are available—carnivorans and rodents—at least one layer receives
mixed input from RGCs of multiple physiological properties (Fig.7.5) (Casagrande
et al. 2009; Preuss 2009; Baldwin and Bourne 2017). In primates, however, the
parallel pathways of visual information rst seen in the retina continue, wherein
magnocellular, parvocellular, and koniocellular inputs discretely segregate within
individual lamina or interlaminar regions of the LGN (Kaas etal. 1978; Kaas and
Preuss 1993; Preuss, 2009). Each layer represents retinal input from just one of the
eyes. Primates have paired magno- and parvocellular layers from each eye, creating
a four-layer system/morphology (Preuss 2009) with a koniocellular distribution
between P and M layers that varies among clades (Kaas etal. 1972; Kaas and Huerta
1988; Kremers etal. 2005; Casagrande etal. 2009). Strepsirrhines have prominent
and distinct koniocellular layers between parvocellular laminae, which some authors
divide and classify differently (Fig.7.5, e.g., Kremers etal. 2005; Casagrande etal.
2009). However, unlike strepsirrhines, haplorhines keep koniocellular distributions
in indistinct and thin interlaminar regions, especially between the ipsi- and
contralateral parvocellular layers (Kremers etal. 2005). Although the polarity of
character evolution remains ambiguous, we may reasonably propose that the clear
koniocellular laminae present in strepsirrhines are primitive and were subsequently
lost in ancestral haplorhines. Instead, diurnal haplorhines display the formation of
interlaminar distributions or, in some cases, add koniocellular input to parvocellular
laminae (Hendry and Casagrande 1996; Hendry and Reid 2000). The haplorhine
parvocellular lamina adjoin and interdigitations of parvocellular leaets develop in
an LGN region in retinotopic register with the central visual eld. A crude allometry
exists whereby substantial enlargement and interdigitations of layers and leaets are
known in larger sized platyrrhines, and to a much greater degree in catarrhines,
especially in hominoids with the unexplained exception of gibbons (Kremers etal.
2005). The interdigitation of the parvocellular leaets results in the “classic” human
six-layer arrangement that medical students nd so difcult to learn.
Both Aotus and Tarsius differ from the diffuse K-cell distribution seen in diurnal
haplorhines (Fig.7.5), instead exhibiting comparatively dense and histologically
distinctive interlaminar collections of koniocellular input within the LGN (Hendry
and Casagrande 1996; Hendry and Reid 2000; Collins etal. 2005; Kremers et al.
2005; Preuss 2009). Owl monkeys differ from tarsiers; the former has a notable K
layer “dividing” the magnocellular and parvocellular layers (e.g., Fig.7.5), whereas
7 Visual System oftheOnly Nocturnal Anthropoid, Aotus: TheOwl Monkey

224
the latter also has a K layer between the outer and inner parvocellular layers (Collins
etal. 2005). However, the heterogeneity of retinal ganglion cell types contributing
to koniocellular input, as well as possible heterogeneity across LGN levels, makes
denitive functional assessments of the emphasis of K-cells in nocturnal haplorhines
elusive (Casagrande 1994; Kremers etal. 2005), since a generalized primate model
of the color processed along each of the three pathways is not yet available
(Casagrande et al. 2009). Owl monkeys differ from other haplorhines with the
reduction, if not absence, of koniocellular input between the parvocellular layers,
which in diurnal haplorhines may include blue-yellow comparisons based on S-cone
input (Hendry and Casagrande 1996; Martin etal. 1997; Hendry and Reid 2000; but
see Casagrande etal. 2009).
The enlargement of the koniocellular input to the interlaminar regions of the
lateral geniculate nucleus in owl monkeys and in tarsiers is intriguing and could
possibly relate to binocular integration. Koniocellular cells in the LGN of marmosets
respond to multiple types of binocular stimuli (Zeater etal. 2015; Belluccini etal.
2019). Belluccini etal. (2019) found multiple K cells exhibiting partial binocular
summative (additive) or facilitative (greater than additive) responses, although they
concluded that binocular summation in marmosets is generally weak and inhibitory.
Aotus lacks the blue-yellow contribution to the K pathway present in diurnal
haplorhines (Dacey and Lee 1994; Hendry and Casagrande 1996; Martin et al.
1997; Hendry and Reid 2000; Martin and Grünert 2013). However, koniocellular
layers in Aotus, as in other primates, receive input from multiple structures, including
Fig. 7.5 (a) The patterns of lamination or layering in the primate dorsal lateral geniculate nucleus
(LGN) vary phylogenetically. In this schematic, layers receiving input from the contralateral eye
are shaded and longer, with length representing the greater representation of the contralateral
visual eld. In most mammals, at least one LGN layer receives mixed input from both eyes,
whereas in primates, input from each eye is segregated into discrete parvo-, magno-, and
koniocellular layers (Kaas and Preuss 1993; Preuss 2009). Strepsirrhine primates possess
histologically distinctive koniocellular layers. In anthropoids, koniocellular input is limited to
smaller interlaminar regions (not shown). Aotus and Tarsius convergently evolved expanded
koniocellular input with one distinctive layer in owl monkeys and two in tarsiers. Based on
diagrams in Kaas etal. (1978), Kaas and Huerta (1988), and Kremers etal. (2005). Inset: transverse
Nissl-stained sections. (b) Mus musculus and (c) Macaca mulatta. From http://www.brainmaps.
org, following Swanson (2012). Location of LGN in mouse is outlined in green dashed line
C. C. Veilleux and C. P. Heesy

225
the superior colliculus, V1, and the retina (Harting etal. 1991; Casagrande and
Boyd 1996; Zeater et al. 2015; Belluccini et al. 2019), and this input has been
hypothesized to improve spatial attention for target selection within the binocular
eld (Casagrande etal. 2005a, b). The relationship between binocular visual eld
overlap (as measured by orbit orientation) and scaling of retinogeniculostriate
pathway sizes appears to be unique to primates among mammals (Barton 2004;
Heesy etal. 2011). Binocular summation improves brightness perception, especially
for dim lights, contrast sensitivity, and visual acuity (Howard and Rogers 1995), and
has been hypothesized to be a key factor for the evolution of larger binocular visual
elds for dim light living or nocturnal animals (Allman 1977; Pettigrew 1978, 1986;
Cartmill 1992; Heesy 2007, 2009; Heesy and Hall 2010). Larger koniocellular
processing in nocturnal owl monkeys and tarsiers may reect a greater exploitation
of binocular summation for targeting salient visual stimuli in a light-limited
environment.
7.4.4 Adaptations: Behavior
Field and lab studies indicate that owl monkeys also exhibit behavioral traits that are
consistent with an emphasis on nocturnal vision. Specically, nocturnal activity is
positively associated with increasing lunar luminosity in all species examined
(Erkert and Gröber 1986; Wright 1989; Fernandez-Duque 2003, 2011; Fernandez-
Duque and Erkert 2006; Fernandez-Duque et al. 2008; Fernandez-Duque et al.
2010; Fernandez-Duque and de la Iglesia 2023 this volume; Link etal. 2023 this
volume). This “lunar philic” behavior means that owl monkeys are most active in
brighter mesopic light conditions where both rods and cones can function. Wild owl
monkeys generally exhibit increased travelling (including longer daily path lengths),
increased feeding, increased social behavior, and overall increased time active
during brighter moonlight (Wright 1989; Fernandez-Duque 2003; Fernandez-
Duque etal. 2008). Wright (1989) further describes lunar-associated increases in
intergroup ghting and intergroup calling. Captive animals, meanwhile, increase
locomotor activity and overall activity in brighter light (e.g., Erkert 1976; Erkert and
Gröber 1986). Brighter moonlight environments may provide more opportunity for
owl monkeys to engage in visual tasks involving spatial acuity or rod/cone color
discrimination. Lunar philic behavior is not unique to owl monkeys; it is also found
in tarsiers and several other primate species (Gursky 2003, see Sect. 7.5.3).
7.4.5 Effects onVisual Function
Visual Acuity Visual acuity is a measure of how well an animal can resolve ne
detail. It is often reported in cycles per degree (cpd), referring to the number of
adjacent black and white bars resolvable in one degree of visual angle (1 black bar
7 Visual System oftheOnly Nocturnal Anthropoid, Aotus: TheOwl Monkey

226
+1 white bar=1cycle). Acuity can be measured using behavioral psychophysical
tests or estimated anatomically using peak cone or RGC densities and eye size
(reviewed in Veilleux 2020). Maximum acuity estimates for owl monkeys using
behavioral (10cpd: Jacobs 1977b) and anatomical methods (8.3cpd: Yamada etal.
2001) are fairly consistent. These values are much lower than the acuity data
available for diurnal haplorhines (e.g., 25–70cpd; Ross 2000; Kirk and Kay 2004;
Veilleux and Kirk 2014). However, also in contrast to diurnal haplorhines, rods
appear to contribute to visual acuity in Aotus (see Sect. 7.4.2.3; Jacobs 1977b,
Yamada etal. 2001). This rod contribution may explain why owl monkeys are able
to maintain fairly consistent maximum acuity estimates across a variety of
illumination levels while human subjects cannot (Jacobs 1977b). In fact, below a
certain light level (~0.006cdm−2), Jacobs (1977b) found that owl monkeys had
higher acuity than human subjects. The evolution of this rod contribution likely
represents an adaptation for maintaining consistent acuity across the dramatic range
of nocturnal light levels owl monkeys encounter in natural habitats.
Color Discrimination While owl monkeys lack SWS cones and consequently
should lack any color discrimination in photopic conditions, early psychophysical
work suggested that they have anomalous (defective) trichromacy (Jacobs 1977a).
It is possible, however, that these early ndings actually represent interactions
between rods and M/LWS cones (Jacobs etal. 1993). Jacobs (1977a) measured
spectral sensitivity in Aotus using behavioral tests at different light levels. At the
lowest level (0.001cdm−2), only rods contributed to the spectral sensitivity function
(resulting in a peak at 500nm), but at higher light levels (4.8 and 19cdm−2, both
considered “photopic”), there was evidence of two peaks in the spectral sensitivity
function, one possibly consistent with rods and one consistent with owl monkey M/
LWS cones. Behavioral tests also suggested color discrimination (Jacobs 1977a).
Subsequent work using electroretinogram icker photometry and much higher light
levels identied the contribution of only the M/LWS cone and no color vision
(Jacobs etal. 1993). Given that owl monkey rods appear to function at higher retinal
light intensity levels than those of diurnal haplorhines (Silveira etal. 2004), the light
levels used by Jacobs in the earlier work may have been low enough to permit rod
function (Jacobs etal. 1993). Data directly demonstrating mesopic level rod-cone
contributions to color contrasts in primates are currently limited to those collected
in humans using psychophysical approaches (Pokorny etal. 2006; Zele etal. 2013;
Zele and Cao 2015). Nonetheless, it is intriguing that rod-cone color discrimination
has been observed in other monochromatic mammals with SWS-cone loss just as in
Aotus. Oppermann etal. (2016) found that two species of harbor seals (Pinnipeda)
lacking SWS cones could make color discriminations in photopic conditions, which
is especially surprising given that only about 1% of their photoreceptor complement
is cones (Peichl and Moutairou 1998).
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227
7.4.6 Adaptations toCathemerality?
Because cathemeral mammals must balance the conicting demands of vision in
bright and dim light conditions, they often exhibit visual features and visual function
intermediate to diurnal and nocturnal taxa (Walls 1942; Kay and Kirk 2000; Arrese
2002; Kirk 2006b; Veilleux and Kirk 2009, 2014; Peichl et al. 2017). Cathemeral
lemurs, for example, possess relative cornea sizes, photoreceptor densities, and
rod:cone ratios that are between those characteristic of diurnal and nocturnal
strepsirrhines (Kirk 2006b; Peichl et al. 2017). Cathemeral mammals may even
exhibit derived adaptations, such as increased pupil mobility, to cope with the wide
variety of light intensities and rapid changes in light intensity they encounter during
diurnal activity, particularly in forested environments (Arrese 2002; Douglas 2018).
Following the description of cathemeral behavior in the Azara’s owl monkeys
(Aotus azarai azarai) of the South American Chaco region (Wright 1989; Fernandez-
Duque 2003), there has been interest in investigating possible evolutionary changes
to the visual system of this Aotus taxon.
Currently, however, there is no evidence of variation in visual structures or genet-
ics between the cathemeral taxon and other nocturnal owl monkeys. Coleman
(2010), for example, found no statistically signicant differences in the skeletal
dimensions of the orbit between the cathemeral A. azarai and nocturnal A. azarai
populations. There are also no differences between cathemeral and nocturnal Aotus
populations in terms of opsin gene variation. Mundy etal. (2016) surveyed M/LWS
opsin gene diversity in 20 cathemeral A. azarai females to explore whether the shift
to diurnal activity has led to the re-evolution of allelic variation and distinct MWS
and LWS cones. They found no variation at the three spectral tuning sites in the M/
LWS gene responsible for color vision variation in primates. Similarly, examination
of the SWS1 opsin gene found that the cathemeral population shared the loss-of-
function mutation common to all Aotus taxa, as well as a second loss-of-function
mutation unique to the southern species group after its divergence from the northern
group (Levenson etal. 2007). Together, these studies indicate that there has been no
re-evolution of color vision or other adaptations for diurnal vision in the cathemeral
population.
7.5 Owl Monkey Visual Systems inaComparative
Evolutionary Framework
As the only nocturnal anthropoid, owl monkey visual features are often discussed in
relation to those observed for diurnal anthropoids. However, it can be useful to
situate Aotus within a broader taxonomic framework to better understand their
visual adaptations. While owl monkeys transitioned to nocturnality ~12–15 MYA
(Setoguchi and Rosenberger 1987), tarsiers are believed to have been nocturnal for
45 MYA, while lorisiforms and nocturnal lemurs have likely maintained nocturnality
7 Visual System oftheOnly Nocturnal Anthropoid, Aotus: TheOwl Monkey

228
since the origin of primates (Heesy and Ross 2001; Rossie etal. 2006; Grifn etal.
2012; Santini etal. 2015). Current evidence suggests that diurnal and cathemeral
lemurs, such as Propithecus and Eulemur, respectively, transitioned to day activity
in the mid to late Miocene (10–20MYA) (Grifn etal. 2012; Santini etal. 2015),
although this has historically been subject to debate (e.g., van Schaik and Kappeler
1996). Overall, cathemeral and diurnal lemur visual features (e.g., eye shape, retinal
morphology) resemble those of cathemeral and diurnal mammals, respectively,
suggesting that these taxa may have inhabited their activity patterns for sufcient
enough time to have adapted visually (Kirk 2004, 2006b; Peichl etal. 2017). Some
authors also argue that the lemur genus Avahi has secondarily transitioned into a
nocturnal activity pattern from a diurnal or cathemeral ancestor, offering a further
potential non-haplorhine comparison to owl monkeys (Ganzhorn etal. 1985; Roos
etal. 2004; Grifn etal. 2012). Unfortunately, there are currently limited comparative
data on Avahi visual traits beyond opsin genes (Veilleux etal. 2013, 2014).
In this section, we revisit several of the owl monkey visual features discussed in
the previous section in a comparative context relative to tarsiers, lorisiforms, and
lemurs. Comparative data are summarized in Table7.1 for representative taxa of
these clades.
7.5.1 Eye Size andShape
Current evidence indicates that (excluding Aotus and Tarsius) eye size does not
actually vary substantially between diurnal and nocturnal primates of similar cranial
size (Kirk 2006a). In fact, many nocturnal strepsirrhines exhibit transverse eye
diameters that are comparable to those of similarly sized diurnal taxa (e.g.,
Cheirogaleus, Nycticebus, Otolemur, Perodicticus: Kirk 2006a). Only a few
nocturnal strepsirrhines exhibit eye sizes relatively larger than comparable diurnal
taxa (Loris, Galago moholi). Even then, eye sizes in owl monkeys and tarsiers were
absolutely and relatively larger than nocturnal strepsirrhines. Kirk (2006a) proposed
that the evolution of relatively large eyes in some nocturnal primates is associated
with selection for increased nocturnal visual acuity, such as for visually guided
faunivory. While the amount of animal prey in the diets of Aotus species is difcult
to quantify, owl monkeys have been observed catching and consuming insects and
vertebrates (Fernandez-Duque 2011; van der Heide etal. 2023 this volume). Thus,
an emphasis on increased nocturnal visual acuity is consistent with other aspects of
owl monkey ecology and visual anatomy.
As mentioned previously, the size of the cornea relative to eye size differs with
light environments across primates, with taxa active in lower light levels exhibiting
relatively larger corneas than those active in higher light levels (Walls 1942; Kirk
2004; Kirk and Kay 2004; Ross and Kirk 2007; Veilleux and Lewis 2011). Among
strepsirrhines, nocturnal species have signicantly larger relative cornea sizes
compared to diurnal species, with cathemeral species falling in between (Table7.1,
Kirk 2004; Ross and Kirk 2007). Tarsiers group with other nocturnal mammals in
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229
relative cornea size; however, Aotus exhibits “unusually small” relative cornea sizes
compared to other nocturnal species. This small cornea size may reect an adaptation
for relatively high acuity nocturnal vision (Kirk 2004); smaller corneae increase
visual acuity by restricting incoming light to comparatively paraxially oriented rays
(Lythgoe 1979; Land and Nilsson 2012). While the small cornea size in owl monkeys
could alternatively reect its recent diurnal ancestry, it is worth noting that Aotus
has been nocturnal likely as long as Propithecus and other lemurs have been diurnal
or cathemeral, and relative cornea size in these taxa has had sufcient time to evolve
to match other diurnal and cathemeral mammals (Kirk 2004, 2006b).
7.5.2 The Retina andRelated Microstructures oftheEye
Rod:Cone Ratios and Photoreceptor Densities As expected for a nocturnal
taxon, owl monkeys have higher rod densities, lower cone densities, and higher
rod:cone ratios than other platyrrhines. For some of these metrics, however, owl
monkeys appear more similar to diurnal or cathemeral lemurs than other nocturnal
primates (Table7.1). Nocturnal strepsirrhines, for example, tend to exhibit much
higher rod densities (~344,000 to 870,000/mm2, with most species studied >450,000/
mm2: Wikler and Rakic 1990; Peichl etal. 2017) than that observed in Aotus
(325,000 to 399,413/mm2: Wikler and Rakic 1990; Yamada etal. 2001; Finlay etal.
2008). Instead, owl monkey rod densities are more similar to those in diurnal
Propithecus (225–370,000/mm2) and cathemeral Eulemur (200–430,000/mm2),
although comparable to tarsiers (Hendrickson et al. 2000; Collins et al. 2005).
Despite the considerable variation in the rod:cone ratios reported for Aotus (see
Sect. 7.4.2.3), overall, the ratios in the central and peripheral retina appear most
similar to those of cathemeral Eulemur (Table7.1) and slightly lower than those
observed in nocturnal strepsirrhines.
Color Vision and Opsin Genes Very interesting differences emerge when com-
paring cone types and opsin genes between owl monkeys and other nocturnal and
cathemeral primate taxa (Table7.1), which have implications for interpreting their
evolutionary history. For example, while owl monkeys experienced opsin loss and
the evolution of monochromatic color vision likely early in their evolutionary his-
tory, the only other nocturnal haplorhine, tarsiers, has maintained SWS cones and
dichromatic color vision through 45 million years of presumed nocturnality
(Hendrickson et al. 2000; Collins et al. 2005). Further, both phylogenetic and
population genetic evidence indicate that tarsiers are under selective pressure to
maintain SWS cone function (Kawamura and Kubotera 2004; Moritz etal. 2017).
Additionally, the presence of spectrally distinct M/LWS opsin alleles in different
tarsier species has led some authors to argue that until the Miocene, early tarsiers
had both hypertrophied eyes and trichromatic color vision, highlighting a potential
role for trichromacy in mesopic conditions (Melin etal. 2013).
7 Visual System oftheOnly Nocturnal Anthropoid, Aotus: TheOwl Monkey

230
Table 7.1 Data comparing fundamental visual and ecological characteristics between owl monkeys and other primates of varying specializations
Activity
pattern
Body mass
(kg)
Eye axial length
(mm)
Relative cornea
size
Peak rod
density
Peak cone
density
Rod:cone ratio
Central
retina
Peripheral
retina
Haplorhines
Aotus trivirgatus N 0.77 19.2–20.0 0.67–0.68 325,000 7000 14:1 93:1
Aotus azarai N/C 1.21 399,413 17,090 24:1 39–40:1
Cebus capucinusaD 3.1 14.1 0.52 174,967 164,062 Rod-freeb15:1–20:1
Callithrix jacchus D 0.35 11.3 0.52 79,102 132,813 Rod-freeb
Tarsius N 0.13 16.1–17.0 0.81 >300,000 14,200
Strepsirrhines
Lemurs
Propithecus
verreauxi
D 3.1 17.7 0.74 370,000 39,000 18:1 23:1
Eulemur avifronsaC 2.13 15.3 0.79 430,000 19,000 28:1 34:1
Microcebus murinus N 0.06 9.2 0.87 630,000 10,900 57:1 200:1
Phaner pallescens N 0.46
Lorisiforms
Nycticebus coucangaN 0.65 15.7 0.77
Otolemur
crassicaudatus
N 1.15 13.4 0.82
Otolemur garnettii N 0.76 450,000 8500 39:1 100:1
Perodicticus potto N 1.04 12.4 0.84 300:1
SWS λmax (nm) M/LWS λmax (nm) Rod architecture Tapetum lucidum Visual acuity
(cpd)
Lunar
behaviorc
Haplorhines
Aotus trivirgatus Lost 543 Intermediate Present 10 Philic
Aotus azarai Lost 543 Intermediate Present 8.3 Philic
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Cebus capucinusa426 530/545/560 Conventional Absent 46.8 n/a
Callithrix jacchus 543/556/563 Conventional Absent 30 n/a
Tarsius 430 543 or 558 Conventional Absent 8.9 Philic
Strepsirrhines
Lemurs
Propithecus
verreauxi
430 543/558 Inverted Present n/a
Eulemur avifronsa413 543/558 Inverted Nonfunctional 5.1 Philic
Microcebus murinus 409 558 Inverted Present 4.2 Philic
Phaner pallescens Lost 543 Philic
Lorisiforms
Nycticebus coucangaLost 543 Inverted Present 3.9–6.5*Phobic
Otolemur
crassicaudatus
Lost 543 Present 4.9
Otolemur garnettii Lost 543 Present Philic
Perodicticus potto Lost 543 Present 4.1 to 4.4
Data sources: body mass (calculated as average of male and female values from Smith and Jungers 1997); eye axial length and relative cornea size (Ross and
Kirk 2007), rod and cone densities [Cebus, Callithrix, A. azarai (Finlay etal. 2008); lemurs (Peichl etal. 2017), A. trivirgatus, Otolemur (Wikler and Rakic
1990); Tarsius (Collins etal. 2005)]; rod:cone ratios [A. trivirgatus and Otolemur (Wikler and Rakic 1990); A. azarai (Yamada etal. 2001), Cebus (Andrade
da Costa and Hokoç 2000); lemurs (Peichl etal. 2017); Perodicticus (Goffart etal. 1976)]; SWS cones (Surridge etal. 2003; Veilleux etal. 2014; Moritz etal.
2017); M/LWS cones [Aotus (Jacobs etal. 1993), Cebus (Hiramatsu etal. 2004); Callithrix (Surridge etal. 2003); Tarsius (Melin etal. 2013); Propithecus
(Veilleux etal. 2016); Eulemur (Veilleux and Bolnick 2009); Phaner (Veilleux, unpublished data); Microcebus, lorisiforms (Tan and Li 1999)]; rod nuclear
architecture (Koga etal. 2017; Joffe etal. 2014); tapetum lucidum (Walls 1942; Goffart etal. 1976; Rodieck 1988; Martin 1990; Peichl etal. 2017); visual
acuity [A. trivirgatus (Jacobs 1977b); A. azarai (Yamada etal. 2001); Cebus (Andrade da Costa and Hokoç 2000); Callithrix (Troilo etal. 1993); Perodicticus
(Coimbra etal. 2016), Nycticebus (estimated from optic foramen area and eye size: Veilleux 2020); Eulemur, Microcebus, Otolemur (Veilleux and Kirk 2009)],
lunar behavior [Aotus (Fernandez-Duque 2011); Tarsius (Gursky 2003); Eulemur (Schwitzer etal. 2007); Microcebus (Deppe etal. 2016); Phaner (Veilleux
unpublished data); Nycticebus (Nash 2007; Starr etal. 2012; Rode-Margono and Nekaris 2014); Otolemur (Nash 2007)
aSome data are for congeners or closely related taxa (e.g., Cebus/Sapajus apella)
bThe fovea of diurnal haplorhines is rod-free and contains only cones
cLunar behavior categorized as lunar “philic” (increasing activity in brighter moonlight) “neutral” (no change in behavior with moonlight level), “phobic”
(decreasing activity in brighter moonlight), or “n/a” (not applicable because species is diurnal). Blanks reect missing data
7 Visual System oftheOnly Nocturnal Anthropoid, Aotus: TheOwl Monkey

232
In contrast to tarsiers, owl monkeys appear to have experienced relaxed selection
for color vision, resulting in the loss of the M/LWS polymorphism and the SWS
cone. A similar SWS cone loss occurred convergently in the ancestor of all
lorisiforms and in some cheirogaleid genera (Table7.1, Kawamura and Kubotera
2004; Tan etal. 2005; Jacobs 2013; Veilleux etal. 2013; Peichl etal. 2017), as well
as in a number of non-primate lineages, including raccoons and kinkajous, which
are sympatric with owl monkeys(Jacobs 2013). While mammalian SWS cone loss
was initially linked exclusively to nocturnality (e.g., Tan etal. 2005), the presence
of functional SWS cones and evidence of selection on the SWS1 opsin gene to
maintain function in other nocturnal taxa indicate that nocturnality is insufcient to
explain SWS cone loss (Kawamura and Kubotera 2004; Perry etal. 2007; Zhao
et al. 2009). Subsequent study of other ecological factors inuencing selective
pressure on the SWS1 opsin gene in nocturnal lemurs found that habitat type was a
crucial factor associated with selection on the gene (Veilleux etal. 2013). Specically,
taxa from closed canopy rainforests impoverished in short-wavelength light
exhibited signatures of relaxed selection leading to the accumulation of harmful
genetic mutations, while taxa from open canopy (or seasonally open canopy) forests
where short-wavelength light is abundant exhibit signatures of purifying selection
to maintain SWS cone function (Veilleux etal. 2013).
The role of visual cues in foraging also likely inuences selection on the spectral
sensitivity of retinal cones. While two species of cathemeral Eulemur exhibit
polymorphic trichromacy (E. avifrons, E. macaco), all other cathemeral Eulemur
are dichromats (Veilleux and Bolnick 2009; Valenta etal. 2016; Jacobs etal. 2019).
It has been hypothesized that the Lemuridae last common ancestor possessed
polymorphic trichromacy, given the presence of the polymorphism in other lemurids
(e.g., Varecia) and in closely related Indriidae, as well as the distribution of distinct
MWS and LWS alleles across dichromat lemurid genera (Veilleux and Bolnick 2009;
Jacobs and Bradley 2016; Jacobs et al. 2019). This hypothesis was given some
support in a recent study employing stochastic character mapping of opsin alleles
across strepsirrhines, suggesting that trichromacy has been lost in at least one
Eulemur species (Jacobs etal. 2019). It is unclear what factors have inuenced the
loss of trichromacy, and it is important to not discount the role of nonadaptive
mechanisms (e.g., bottlenecks, genetic drift) in the xation of opsin alleles (Jacobs
and Bradley 2016). Visual modeling of food detection for E. fulvus in the dry forest
at Ankarafantsika found that the observed MWS-type dichromacy is as good as
trichromacy at detecting food items in nocturnal light environments using chromatic
or luminance cues (Valenta et al. 2016), which may lead to relaxed selection for
maintaining the polymorphism. In the eastern rainforest, E. rubriventer are LWS-
type dichromats, which, while not as good as trichromacy at detecting food items
using chromatic cues, was modeled as being a better phenotype for detecting food
items using luminance cues at night (Jacobs etal. 2019). These results led Jacobs
etal. (2019) to propose that luminance cues may play an important role in the dim
light conditions in which Eulemur rubriventer often forages, possibly resulting in
selection against trichromacy. A similar emphasis on luminance cues over chromatic
cues in the context of exudativory has been offered to explain the evolution of
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233
monochromacy in ancestral lorisiforms and in cheirogaleids (Moritz and Dominy
2010; Veilleux etal. 2013; Moritz 2015; Veilleux 2020).
In the context of owl monkey visual evolution, the loss of the SWS cone is con-
sistent with the hypothesis that Aotus initially evolved in closed canopy forests and
only more recently moved into open canopy habitats (Babb etal. 2011). In this early
period of owl monkey evolution, the limited availability of short-wavelength light in
the closed canopy may have led to relaxed selection for color vision and increased
harmful mutations in the SWS1 opsin gene. Moreover, rod-cone interactions may
have been sufcient for detecting relevant chromatic cues, permitting relaxed selec-
tion on the SWS cone. There are currently no data on the spectral reectances of
Aotus foods or the importance of luminance versus chromatic cues for detecting
those foods in twilight or nocturnal environments. This data would allow research-
ers to investigate the importance of rod-cone color vision as well as whether owl
monkeys may have experienced selection for monochromacy, as proposed for pri-
mate exudate feeders. The peak spectral sensitivity of owl monkey M/LWS cones is
identical to that of other primate cone monochromats across different clades
(Table7.1), which may indicate that a cone with ~543nm peak is particularly rele-
vant to species lacking SWS cones. However, comparison across nocturnal mam-
mals indicates that non-primates lacking SWS cones can vary in M/LWS peak
spectral sensitivities (Veilleux and Cummings 2012).
Rod Nuclear Architecture Owl monkeys are thus far unique among mammals in
having re-evolved a centrally located heterochromatin block in the nucleus of their
rods, which may act as a microlens to increase the light-capturing ability of the eye
(Joffe etal. 2014; Nishihara et al. 2018). All strepsirrhines, regardless of activity
pattern, possess the standard “nocturnal mammal” inverted rod nuclear architecture
(Table7.1, Joffe etal. 2014). The retention of this inverted pattern even among taxa
like Propithecus that may have been diurnal since the mid-Miocene (and have
evolved other diurnal visual features) may indicate a possible benet to maintaining
increased rod sensitivity in these taxa, especially considering the inverted nuclear
architecture is disadvantageous for cellular function (Feodorova etal. 2020). Diurnal
strepsirrhines also retain a tapetum lucidum (Peichl etal. 2017) while being strictly
diurnal behaviorally (Erkert and Kappeler 2004). By contrast, despite a long
evolutionary period of nocturnality, tarsiers have retained a conventional diurnal rod
architecture from their diurnal haplorhine ancestor (Joffe etal. 2014). Tarsiers thus
offer an interesting counterpoint to owl monkeys, which, while nocturnal for roughly
half the amount of evolutionary time, have clearly experienced selection to re-evolve
some form of inverted architecture. Possibly other features of tarsier eyes (huge
size, substantially longer rod outer segments to facilitate more light absorption
compared to Aotus), or increased activity in mesopic conditions (e.g., bright
moonlight, twilight), may have allowed them to maintain the conventional rod
architecture (Joffe etal. 2014).
Fovea and Tapetum Lucidum These two eye structures may help unravel the
divergent paths to nocturnality taken by owl monkeys and tarsiers, because animals
7 Visual System oftheOnly Nocturnal Anthropoid, Aotus: TheOwl Monkey

234
cannot easily utilize both simultaneously. Tapeta are fundamental nocturnal
adaptations and have evolved independently in vertebrates multiple times, including
in mammals, because of their extreme usefulness in creating an image when
collecting sufcient light to do so poses a major challenge (Nicol 1981). Any photon
(a precious commodity to a vision-dependent nocturnal animal) missed by the
photoreceptors on its rst pass through the retina bounces back from this reective
layer for a second chance to trigger a transduction event and contribute to creating
an image. However, all the resultant light scatter and glare created by bouncing light
around the retina greatly diminishes the quality of the image, making the usefulness
of a high acuity specialization like the fovea obsolete. The presence of a tapetum
brosum unique to owl monkeys (Sect. 7.4.2.1) awaits further anatomical study, but
its presence might explain the loss of a useful fovea retained from their diurnal
ancestors. If conrmed, the presence of a tapetum in Aotus would again offer an
interesting counterpoint to the other nocturnal haplorhine, tarsiers, who took a
divergent road to nocturnality. Like other haplorhines, tarsiers lack a tapetum
lucidum (Martin 1990; Ross 2000; Heesy and Ross 2001) and have a heavily
pigmented retinal epithelium, the presence of which precludes the presence of a
tapetum, since a tapetum would require an unpigmented layer (Hendrickson etal.
2000). Tarsiers probably increased sensitivity in dim light by developing extremely
large eyes with longer rod outer segments, retaining their still-useful foveae,
whereas owl monkeys combined eye size, intermediate rod nuclear architecture, and
a tapetum; the latter probably rendering their possibly absent possibly
underdeveloped, foveae unnecessary. Strepsirrhines do not possess a fovea, and
most—including diurnal taxa like Propithecus and Indri—share a tapetum lucidum
composed of crystalline riboavin (Pirie 1959; Dartnall etal. 1965; Coimbra etal.
2016; Peichl etal. 2017). Interestingly, at least two lemur genera (Varecia, Eulemur)
are suggested to have lost the tapetum (Kirk and Kay 2004), although some
researchers disagree (e.g., Schwitzer etal. 2007). Recent anatomical study found
that Eulemur species do have tapeta, which are occluded by a light brown pigment
epithelium that may incompletely block light reectance (Peichl etal. 2017). This
results in an interesting paradox in lemurs, where the tapetum has been lost in
cathemeral species—which would be assumed to benet from a tapetum—but
retained in diurnal species.
7.5.3 Visual Function andBehavior
Visual Acuity While owl monkeys exhibit substantially lower visual acuity rela-
tive to diurnal haplorhines (8.3–10cpd vs. 25–70cpd, respectively), their maximum
photopic acuity remains fairly high in a comparative context (Table7.1 and Fig.7.6).
All strepsirrhines thus far measured have acuity values between 2.8cpd and 7cpd
(Veilleux and Kirk 2009; Coimbra et al. 2016; Veilleux 2020). In fact, looking
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across mammals, only a handful of non-haplorhines have visual acuity higher than
those estimated for owl monkeys—primarily large-bodied or predatory animals
such as cheetahs, wolves, horses, and deer (Veilleux and Kirk 2014). Aotus acuity is
comparable to that seen in cathemeral and diurnal mammals, including kangaroos
(10.28 cpd), camels (10 cpd), hyenas (8.4 cpd), and lynxes (8 cpd). Like owl
monkeys, tarsiers also exhibit higher visual acuity than strepsirrhines (8.9 cpd,
Veilleux and Kirk 2009).
No other study has tested acuity in primates at different light levels like Jacobs’s
(1977b) work with Aotus (and humans), making it difcult to compare primate
visual function at mesopic light levels. However, Jacobs’s data demonstrate that owl
monkeys maintain their relatively high acuity into moonlight levels (0.01–1.4 cd/
m2) and still exhibit rod-based acuity levels in starlight illumination (0.001cd/m2)
comparable to the photopic acuity achieved by cathemeral lemurs (~5cpd). This
mesopic acuity in Aotus is also superior to cats (Jacobs 1977b; Blake 1988; Yamada
etal. 2001), the only other well-studied non-primate or non-rodent model for which
comparable data are available. Owl monkey dim light acuity is higher than the
maximum acuity possible under the brightest conditions for most nocturnal
strepsirrhines (Table7.1). Rods likely contribute to these higher acuity functions,
given the substantive rod contribution to the P pathway in Aotus at higher retinal
light intensity values (Silveira etal. 2004). Rod functionality at photopic light levels
has been shown in mice and may be more widespread than previously believed
(Tikidji-Hamburyan etal. 2017; reviewed in Kelber 2018). Thus, from a comparative
mammalian perspective, owl monkeys exhibit relatively high visual acuity in both
diurnal and nocturnal light environments.
Visual Behavior While all owl monkeys seem to exhibit lunar philic behavior—
increasing activity with brighter nocturnal illumination (Fernandez-Duque 2011;
Fernandez-Duque et al. 2023 this volume; Link et al. 2023 this volume)—this
pattern of behavior is not the norm across mammals. In fact, most mammals are
“lunar phobic,” meaning that they decrease activity in brighter moonlight or shift to
microhabitats with denser cover (reviewed in Bearder etal. 2006; Nash 2007, but
see Huck etal. 2016). In general, lunar phobia may reect an adaptation for reducing
predation risk (Nash 2007). Among nocturnal primates, however, lunar philia is
more common (Table7.1), possibly relating to the increased emphasis on the use of
vision for foraging and/or predator detection in primates (Table7.1, Bearder etal.
2006; Nash 2007). Many nocturnal primates increase activity, call more frequently,
or travel farther during higher nocturnal light levels. However, there are some taxa
that either seem to avoid bright moonlight (Nycticebus: Nash 2007; Starr etal. 2012;
Rode-Margono and Nekaris 2014) or show no effect of nocturnal light intensity on
behavior (Lepilemur: Nash 2007). Thus, the presence of lunar philia in owl monkeys
is not unique across primates, but likely corresponds to an increased emphasis on
high acuity nocturnal vision.
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236
7.6 Conclusion
With the transition to diurnality in the early Eocene, haplorhines evolved multiple
unique innovations compared to other mammals to support extremely high visual
acuity and enhanced color vision (Kirk and Kay 2004). Then, in the mid-Miocene,
the ancestor of owl monkeys probably shifted back to a nocturnal niche from this
highly derived haplorhine condition. Even with the shift to dim light visual
environments, Aotus maintained a sensory emphasis on vision and has likely
experienced selection for increased nocturnal visual acuity. Our synthesis of
available evidence strongly indicates that owl monkeys have evolved a number of
derived adaptations for dim light vision in their gross eye morphology, opsin genes,
retinal cells and structure, and brain organization. Some of these features represent
novel innovations not observed in any other mammal (e.g., OwlRep and re-evolved
inverted rod nuclear architecture) or primate (e.g., tapetum brosum). It is interesting
that tarsiers, the only other nocturnal haplorhine, followed a different evolutionary
path to dim light vision, despite starting from the same highly derived haplorhine
condition. Tarsiers have had nocturnal activity patterns for nearly twice as long as
owl monkeys, yet retain many “diurnal” haplorhine visual traits, including SWS
cones and color vision, conventional “diurnal” rod nuclear architecture, and a retina
fovea. Lacking a tapetum and derived rod nuclear architecture, tarsiers appear to
increase visual sensitivity in dim light through extremely large eyes and longer rod
outer segments. The two lineages are often grouped together, implying similar
selective pressures for nocturnal vision, and do share some convergent adaptations
to dim light (e.g., distinct koniocellular layers, large eyes, lunar philic behavior).
However, it is also important to emphasize their numerous differences in dim light
adaptations. Future visual ecology work should explore how these genera vary in
chromatic and luminance target detection, microhabitat usage, chronobiology, and
light environments to begin untangling factors driving this anatomical variation.
While tarsiers have been a recent focus in visual ecology (e.g., Melin etal. 2013;
Moritz etal. 2014; Moritz et al. 2017), very little work has examined the visual
ecology of owl monkeys, and much is still unknown. Vital ecological data are
needed, particularly on the spectral reectances of preferred foods, microhabitat
preferences and light environments, more ne-grained detail on lunar philic
behaviors (e.g., do visually guided behaviors increase in brighter light?), and the
role of vision as well as other sensory systems while foraging, moving, and
socializing (Spence-Aizenberg etal. 2023 this volume). Owl monkeys may also
particularly benet from a community-level approach (e.g., Veilleux etal. 2021),
wherein Aotus sensory traits and behavior could be compared with sympatric
nocturnal or cathemeral mammalian competitors, such as didelphid marsupials,
procyonids, or rodents, as well as diurnal primates. There are also still many
unknowns regarding the extent of individual-, population-, and species-level
variation in Aotus visual systems (e.g., presence of fovea).
As our review demonstrates, owl monkeys seem to be well suited to contend with
the dramatic variation in light intensity and spectral quality encountered in natural
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237
forest habitats. In particular, features of their visual system appear to extend the
range of light intensities considered “mesopic” for owl monkeys, thereby decreasing
the threshold for cone function and increasing the threshold for rod function relative
to diurnal haplorhines (Silveira 2004). As a consequence, unlike diurnal primates,
owl monkeys are able to maintain a fairly consistent level of visual acuity across a
range of light environments (Jacobs 1977b) while also retaining possible rod-cone
mediated color vision into what would be considered “photopic” environments for
diurnal monkeys (Jacobs 1977a). This unique extension of mesopic conditions may
offer a visual basis for the behavioral exibility observed in the cathemeral
populations of the South American Chaco region. It is currently unclear whether
this extension of mesopic conditions is common across other night-active primates
Fig. 7.6 Approximation of how a pair of owl monkeys would appear to different primate taxa,
assuming a viewing distance of 2m. (a) Trichromat human with 70cpd acuity, (b) monochromat
owl monkey with 10cpd, (c) dichromat tarsier with 8.9 cpd, and (d) monochromat potto with
4.1 cpd. (Comparative images created using AcuityView (Caves and Johnsen 2018). Original
photograph of Aotus vociferans: ©Napowildlifecenter/Wikimedia Commons/CC-BY-SA-3.0)
7 Visual System oftheOnly Nocturnal Anthropoid, Aotus: TheOwl Monkey

238
or whether it is a result of the owl monkey’s unique evolutionary history. Aotus
visual anatomy and function have been particularly well studied due to its status as
a comparative model in biomedical research—corresponding data from captive and
eld studies on the neuroanatomy, visual function, ecology, and behavior of
nocturnal and cathemeral strepsirrhines (and other euroarchontans) are needed in
order to properly characterize the range of mesopic visual environments utilized by
primates and identify adaptations for nocturnal high acuity vision.
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