Introduction
The activity periods of non-human primates is an extremely important subject area. Numerous correlations exist between activity period and morphology, physiology, and social structure. For example, it is fairly well established that nocturnal primate species have relatively larger orbits and eyeballs than do diurnal species, which is linked as much to their habitat as it is to light absorption, i.e. other nocturnal mammals do not have larger eyes than diurnal mammals (Martin 1990;Falk 2000;Schultz 1940). Also, many nocturnal species, excluding Tarsius, retain a tapetum lucidum and lack a central fovea in the retina, instead having an area centralis (Ankel-Simons 1983;Falk 2000;Rowe 1996). One of the best examples of how morphology can be influenced by a primates activity period is the genus Aotus. This group of anthropoids has both a tapetum lucidum and a predominately rod based retina, which are both quantified as nocturnal adaptations (Ankel-Simons 2000). It is also generally accepted that the senses of smell and hearing are more important than vision to nocturnal primates, and this is seen structurally in the large flexible ears and wet rhinarium of many nocturnal prosimians (Falk 2000; Jurmain, et. al., 2003). Social structure can also be modified based on activity period. For example, many nocturnal lemurs are solitary foragers (Jurmain 2003).
Activity periods can also be influenced by environmental and physiological factors. Engqvist (2000) notes that cathemeral activity may be an adaptation to a folivoris diet, and it is hypothesized that the Lorisidae became nocturnal to avoid competition and predation (Falk 2000). Although all this information exists about activity period correlates, literature that directly quantifies the differences in the morphology of the anterior eye orbit between diurnal, cathemeral, and nocturnal primates is scarce (Schultz 1940). A few studies quantify the relationship between body size and orbital size in primates, however, little information exists on how to calculate body size based on orbit size within an established activity period (Kay et. al., 2000; Schultz 1940).
Anterior orbital morphology is of interest for several reasons. First, this is the region through which optical signals must pass, and orbital shape would presumably have an impact on optical processing. Secondly, the anterior orbit plays a major part in a primate��s appearance. In other words, identification of a species could be facilitated by investigation into the anterior orbital morphology. Finally, cranial morphology, and specifically orbital morphology, is one of the primary means of linking fossils to known extant species and orbital dimensions have known functional correlates (Kay and Kirk 2000; Tuttle 1972, VIII). Steudel (1985) discusses many of the problems with using other anatomical regions for paleontological extrapolation, and notes a relatively high correlation coefficient between both orbital width and height, and skeletal weight. There are also problems with paleontological extrapolation based on the eye orbit. This area is often quite fragile and certain portions may be missing (Bass 1995). However, with ever increasing sophistication in paleontological techniques, more and more complete extinct primates skulls are being excavated. Therefore, anterior orbital morphology needs to be quantified for use by primatologists and paleoprimateologists, both in the field and in the laboratory. This study compares the anterior orbital morphology of nocturnal, cathemeral, and diurnal primates.
Materials and Methods
Measurements
This analysis compares the orbital indices and orbital area of nocturnal, cathemeral, and diurnal primates. The orbital index was calculated by multiplying the orbital height by one hundred and dividing the sum by the orbital breadth. The orbital area was calculated by multiplying the orbital height by the orbital breadth. An orbital area to body weight ratio was calculated by dividing the orbital area by the average body weight and multiplying the sum by one hundred. Orbital breadth is here defined as a measurement of the maximum width of the orbit using the lateral anterior border of the orbit as a fixed point. The orbital height is a measurement of the maximum distance between the inferior and superior borders of the orbit using the middle of the inferior border as a fixed point. These measurements were taken on the left orbit of the sample primate skulls whenever possible. Measurements were taken with a sliding caliper and were recorded in centimeters. For orbital area correlation and regression analysis, the body weight of each species was estimated following average species weights given by Rowe (1996). The sex of the sample primate was matched to the body weight estimates whenever possible, and all weights are averages, i.e. they are not the actual weight of the sample skulls.
Statistics
For the orbital indices, several statistical methods were implemented. Ninety five percent confidence intervals were calculated for each of the three activity periods. Histograms were then created for each of the three activity periods using a class width of one index point. A single factor analysis of variance (ANOVA) was then implemented using activity period as the treatment. F-tests were conducted to compare the variation between the three activity periods two samples at a time. Two sample t-tests were then implemented to find rank and order among the activity periods.
Correlation and regression methods were conducted for each of the activity periods. This was to see, (A) if orbital area has a correlation with body size, and (B) to find a regression equation to estimate body weight based on orbital area, or vice versa. Student T tests were also conducted to see if the orbital area to body weight ratios statistically differed between the three activity periods.
Statistical tests were conducted with a Texas Instrument number 83 and Microsoft Excel. Graphs were created using the Microsoft Excel program. All tests were conducted with an �� of .05.
Sample
The sample used in this study is located in The Field Museum of Natural History (FMNH). Lists of all species used in this study can be found in appendix A (Pg. 13) along with descriptive statistics, measurement values, and non-parametric identification information.
Results (Appendix A, Tables 1-3)
Orbital Indices
Diurnal primate orbital indices range from 74.19 to 114.29 with a mean of 93.77 and a standard deviation of 9.236 (Figure 1, Pg. 10). Nocturnal primate orbital indices range from 88.24 to 112.5 with a mean of 100.46 and a standard deviation of 6.458 (Figure 2, Pg. 10). Cathemeral primate orbital indices range form 86.34 to 107.14 with a mean of 95.87 and a standard deviation of 9.48 (Figure 3, Pg. 11).
This study showed that, with 95% confidence, (A) the true mean of diurnal primate orbital indices is between 91.198 and 96.34, (B) the true mean of nocturnal primate orbital indices is between 97.901 and 103.01, and (C) the true mean of cathemeral primates orbital indices is between 80.793 and 110.95.
F-tests showed that the variance in nocturnal primates orbital indices is significantly less than the variance found in diurnal primate orbital indices. The probability that nocturnal and diurnal primates orbital indices have the same variance is 0.03198. The orbital index variance in cathemeral primates did not differ significantly from the variance in either diurnal or nocturnal primates.
The single factor analysis of variance showed that there was a statistically significant difference between the mean orbital indices for the three activity periods. There is a probability of .005426 that the three activity periods have the same means.
The Student T tests showed a significant statistical difference between the orbital indices of diurnal and nocturnal primates. There is sufficient sample evidence to conclude that nocturnal primates have a higher mean orbital index than do diurnal species. There is a probability of .000182 that diurnal and nocturnal primates have an equal mean orbital index. The mean orbital index of cathemeral primates did not significantly differ from either nocturnal or diurnal primates.
Orbital Area
Orbital areas in diurnal primates range from .72 to 20 cm2 with a mean of 4.52 cm2 and a standard deviation of 3.531 cm2. Orbital areas in nocturnal primates range from 1.1 to 5.52 cm2 with a mean of 3.20 cm2 and a standard deviation of 1.027 cm2. Cathemeral primates orbital areas range from 2.1 to 4.18 cm2 with mean of 3.47 cm2 and a standard deviation of .945 cm2.
In diurnal primates, orbital area to body weight ratios ranged from 0.0126 to 0.5538 with an average of 0.2033 and a standard deviation of 0.1293. In nocturnal primates this ratio ranged from 0.2055 to 3.4632 with a mean of 0.8740 and a standard deviation of 0.7738. In cathemeral primates the ratio ranged from 0.1551 to 0.2294 with a mean of 0.1843 and a standard deviation of 0.03199. The student t tests showed that there was a statistically significant difference between the orbital area to body weight ratio in nocturnal and diurnal primates as well as between nocturnal and cathemeral primates. However, cathemeral primates could not be distinguished from diurnal primates on the basis of this ratio. The probability that nocturnal and diurnal primates have the same mean orbital area to body weight ratio is 0.000059968148. The probability that nocturnal and cathemeral primates have the same mean orbital area is 0.000045728234.
This study showed that, with 95% confidence, the true mean of the orbital area to body weight ratio for diurnal primates is between .16132 and .23691. For nocturnal primates, the true mean of this ratio is between .56766 and 1.1799, and for cathemeral primates the true mean is between .13335 and .23516. Based on this sample, there is sufficient evidence to conclude that nocturnal primates have a higher orbit to body weight ratio than do diurnal or cathemeral primates.
Statistically significant positive correlations were found between orbital area and body weight in all three activity periods. The Pearson product moment correlation coefficient��s are as follows (with critical values in parentheses): diurnal r = .878 (.294), nocturnal r = .691 (.396), cathemeral r = .968 (.950). The regression equation, where y equals body weight and x equals orbital area, for diurnal primates is y=1794.95681x - 2744.232514 (Figure 4, Pg. 11, n=4 excluded for lack of information, n=3 excluded as outliers, i.e. Pongo, Gorilla, Pan; see appendix A, Pg. 13). For nocturnal primates the regression equation is y=382.5684767x - 563.0943536 (Figure 5, Pg.12), and for cathemeral primates the regression equation is y=728.3242497x - 556.1601463 (Figure 6, Pg. 12).
Discussion
That nocturnal primates have higher mean orbital indices when compared to diurnal primates is partially explained by eye volume relative to orbit size. Several students of primate eye morphology note that nocturnal species consistently have higher eye/orbit ratios than do diurnal primates, which causes the eyeball to protrude from the orbit and the orbit proper to be displaced posteriorly in respect to the eyeball (Kay et. al., 2000; Schultz 1940). This leads to a flaring of the anterior orbit, which is displaced to the medial aspect of the eyeball. By being displaced to the medial aspect of the eyeball, the anterior orbit is forced to take on the relative shape of the medial aspect of the eyeball, i.e. it must be rounded. This is why the confidence interval for the orbital index of nocturnal primates is much closer to 100, or more mesoconchic, than the diurnal species and also why there is less variation in the nocturnal primate orbital indices. In diurnal primates the eye/orbit ratio is much smaller, meaning the eyeball in enclosed partially on the anterior side by a bony ring (Kay et. al., 2000; Schultz 1940). The relationship between the eye shape and activity period is harder to explain for diurnal species than it is for nocturnal species. The confidence interval for diurnal species is significantly lower than 100, meaning they are more chamaeconchic than nocturnal species. This may be due to the scaling and the effects of size on the eyeball, light filtering, or numerous other possibilities. That cathemeral primates cannot be distinguished from either nocturnal or diurnal primates in respect to their orbital index is not terribly surprising, given that this problem has been documented by several students of eye morphology for different orbital indices than the type used here as well as for orbital diameter (Martin 1990;Donati, et. al., 2001;Kay, et. al. 2000). This is possibly due to the fact that ��cathemeral�� primates are not necessarily cathemeral at the species levels. It is possible the cathemeral activity is only an adaptation to environmental conditions, such as luminosity, and temperature or to cosmic forces such as the lunar cycles (Donati , et. al., 2001). In other words, cathemerality may be a secondary adaptation within a species. Further quantification of cathemeral activity and its functional correlates may help resolve this problem.
The posterior displacement of the orbit proper also partially explains the higher relative anterior orbital area in nocturnal primates in comparison to diurnal primates. The posterior displacement of the orbit in nocturnal primates causes the anterior orbit to conform to the medial aspect of the eyeball, as previously discussed. In diurnal species, the lower eye to orbit ratio allows the anterior orbit to conform to the anterior aspect of the eyeball. Since the diameter of the medial aspect of an eyeball must be greater than then the diameter of the anterior aspect of an eyeball, the relative area of an orbit that conforms to the medial aspect of an eyeball must also be greater than the relative area of an orbit which conforms to the anterior aspect of an eyeball. In other words, it is the extreme size of the eyeball, which causes the posterior displacement of the orbit proper in relation to the eyeball, in nocturnal species that causes the relative anterior orbital area to be greater than the relative anterior orbital area of diurnal species (see Schultz 1940).
This study approached the subject of correlation and regression estimation between body weight and orbital area differently than most other studies of eye morphology. Most of the literature quantifies the relationship between body size and eye/orbit size for primates in general (Kay et. al., 2000; Schultz 1940). By relating the correlation and regression to the activity period, this study offers another method for checking body weight estimates in extant species. If these equations prove to be useful in extant species, they can easily be modified for extinct species.
To summarize, this study found that activity period could be estimated based on the morphological shape of the eye orbit. Ninety five percent confidence intervals were calculated for the orbital indices and the orbital area to body weight ratio for each of the three activity periods. Nocturnal species have a statistically higher mean orbital index than do diurnal species, but cathemeral species could not be distinguished from nocturnal or diurnal species. Nocturnal primates also have a statistically higher orbital area to body weight ratio than cathemeral or diurnal primates, however cathemeral and diurnal primates did not differ significantly in this respect. Furthermore, this study quantifies the correlation between orbital area and body weight within diurnal, cathemeral, and nocturnal activity periods. Regression equations were calculated to estimate body weight from orbital area for each activity period, with specific focus on relatively small-bodied primates.
Further quantification of these variables with larger sample sizes, as well as intraspecific analysis of anterior orbital morphology are important areas for future research. Also non-osteological analysis of vision in primates and the synthesis of this information with the current osteological variables is an important area of research.
Acknowledgments
I would like to thank Dr. Davis for getting me access to FMNH and helping with the measurement process.
Appendix A
Table 1
Nocturnal N=27
Genus Species sex orbital height orbital width orbital index orbital area Body weight
Arctocebus calabarensis m 1.5 1.4 107.14 2.1 365.5
Loris tardigradus m 1.7 1.6 106.25 2.72 193.5
Nycticebus coucang m 2 1.8 111.11 3.6 420
" pygmaeus m 1.6 1.7 94.12 2.72 462
Perodicticus potto m 1.8 1.6 112.50 2.88 1225
Euoticus elegantus ? 1.8 1.8 100.00 3.24 271
Galago alleni f 1.7 1.8 94.44 3.06 314
" matschiei f 1.5 1.6 93.75 2.4 210
" moholi f 1.5 1.4 107.14 2.1 188
" senegalensis m 1.6 1.5 106.67 2.4 210
otolemur crassicausatus m 1.9 2 95.00 3.8 1495
" garnettii m 1.8 1.9 94.74 3.42 822
Cheirogaleus major f 1.5 1.5 100.00 2.25 352.5
" medius f 1.2 1.2 100.00 1.44 179.5
Microcebus rufus f 1.1 1 110.00 1.1 49
Lepilemur mustelinus m 1.5 1.7 88.24 2.55 593.8
Avahi laniger m 1.7 1.7 100.00 2.89 1033
Daubentonia madagascarensis? 2.4 2.3 104.35 5.52 2686.5
Tarsius bancanus ? 2 2 100.00 4 115.5
" syrichta m 1.8 1.9 94.74 3.42 134
Aotus nigriceps f 2 2.2 90.91 4.4 940
" infulatus m 2 2 100.00 4 937.5
" azarai f 2.1 2 105.00 4.2 940
" lemurinus m 2.2 2.3 95.65 5.06 950
" vociferans f 1.9 1.8 105.56 3.42 920
" nancymaae f 1.9 2 95.00 3.8 940
" miconax m 2 2 100.00 4 937.5
Averages 1.77 1.77 100.46 3.20 662.40
Standard deviation 0.292 0.313 6.458 1.027 568.587
95% interval 97.901<��<103.01
N= 27
Table 2
Cathemeral N=4
Genus Species sex orbital height orbital width orbital index orbital area Body weight
Eulemur fulvus ? 1.8 2 90 3.6 2321
" macaco ? 1.9 2.2 86.34 4.18 2445
" rubriventer ? 2 2 100 4 2203
Hapalemur griseus ? 1.5 1.4 107.14 2.1 915.5
Averages 1.80 1.90 95.87 3.47 1971.13
Standard Deviation 0.216 0.346 9.48 0.945 710.65233
95% interval 80.793���݃�110.95
Table 3
Diurnal N=52
Genus Species sex orbital height orbital width orbital index orbital area body weight
Lemur catta m 1.8 1.8 100 3.24 2705
Varecia variegata m 2 2.1 95.24 4.2 3471
Propithecus verreauxi ? 2 2.1 95.24 4.2 3558.5
Callimico goeldii m 1.2 1.3 92.31 1.56 467.5
Callithrix argentata m 1.1 1.1 100 1.21 357
" humeralifer m 1.1 1.2 91.67 1.32 280
" jacchus m 1 1.2 83.33 1.2 256
" pygmaea m 0.8 0.9 88.89 0.72 130
Saguinus bicolor f 1.1 1.3 84.62 1.43 430
" fuscicollis f 1 1.2 83.33 1.2 403
" geoffroyi m 1.1 1.2 91.67 1.32 546
" imperator m 1 1.2 83.33 1.2 450
" labiatus f 1.1 1.1 100 1.21 455
" midas f 1.1 1.3 84.62 1.43 432
" mystax f 1.2 1.3 92.31 1.56 574
" oedipus f 1 1.2 83.33 1.2 430
Leontopithecus rosalia ? 1.2 1.3 92.31 1.56 577.5
Callicebus brunneus m 1.7 1.6 106.25 2.72 845
" caligatus m 1.8 1.6 112.5 2.88 na
" cupreus m 1.6 1.6 100 2.56 1163
" donacophilus f 1.6 1.5 106.67 2.4 800
" hoffmannsi m 1.5 1.8 83.33 2.7 920
" moloch f 1.6 1.8 88.89 2.88 860
Cebus albifrons f 2.2 2.3 95.65 5.29 1814
" apella m 2.2 2 110 4.4 3050
" capucinus m 2.4 2.1 114.29 5.04 3868
Saimiri boliviensis f 1.5 1.4 107.14 2.1 800
" scireus m 1.7 1.5 113.33 2.55 852
Pithecia pithecia m 2 2.3 86.96 4.6 1732
Chiropotes satanas f 2.5 2.4 104.17 6 2600
Cacajao calvus m 2.5 2.4 104.17 6 3450
Alouatta seniculus m 2.5 2.7 92.59 6.75 5600
Ateles Spp. f 2.5 2.7 92.59 6.75 na
Lagothrix lagotricha m 2.4 2.6 92.31 6.24 6800
Macaca arctoides m 2.5 2.8 89.29 7 10050
" assamensis f 2.2 2.4 91.67 5.28 6750
" fascicularis f 2.3 2.4 95.83 5.52 4100
" mulatta m 2.6 2.6 100 6.76 8250
Papio anubis m 2.3 3.1 74.19 7.13 28414
Theropithecus gelada f 2.1 2.4 87.5 5.04 11700
Cercocebus Spp. ? 2.3 2.4 95.83 5.52 na
Chlorocebus aethiops m 2.1 2.5 84 5.25 4582
Erythrocebus patas m 2.4 2.5 96 6 10000
Cercopithecus diana f 2.1 2.4 87.5 5.04 5400
Colobus guereza m 2.4 2.6 92.31 6.24 13500
Presbytis obscura m 2.4 2.3 104.35 5.52 na
Pygathrix roxellana f 2.2 2.5 88 5.5 8250
Nasalis larvatus f 2.2 2.3 95.65 5.06 10000
Hylobates lar f 2.3 2.5 92 5.75 5600
Pongo pygmaeus m 3.8 4.2 90.48 15.96 77500
Gorilla gorilla m 4 5 80 20 159200
Pan troglodytes ? 2.9 3.7 78.38 10.73 50000
Averages 1.93 2.07 93.77 4.52 51758.33
Standard deviation 0.689 0.810 9.236 3.531 59961.258
95% t interval 91.198<�݃������|����
Catalogue Numbers (Table 4)
nocturnal Diurnal
Genus Species FMNH Cat. # Genus Species FMNH Cat #
Arctocebus calabarensis FMNH 99360 Lemur catta FMNH 85134
Loris tardigradus FMNH 95024 Varecia variegata FMNH 147987
Nycticebus coucang FMNH 37988 Propithecus verreauxi FMNH 8344
" pygmaeus FMNH 32499 Callimico goeldii FMNH 98034
Perodicticus potto FMNH 44393 Callithrix argentata FMNH 92177
Euoticus elegantus " humeralifer FMNH 50830
Galago alleni FMNH 43730 " jacchus FMNH 121295
" matschiei FMNH 148985 " pygmaea FMNH 71003
" moholi FMNH 78745 Saguinus bicolor FMNH 20133
" senegalensis FMNH 153086 " fuscicollis FMNH 50848
otolemur crassicausatus FMNH 96274 " geoffroyi FMNH 69951
" garnettii FMNH 153090 " imperator FMNH 50857
Cheirogaleus major FMNH 85144 " labiatus FMNH 58801
" medius FMNH 147986 " midas FMNH 93236
Microcebus rufus FMNH 85863 " mystax FMNH 50845
Lepilemur mustelinus FMNH 5658 " oedipus FMNH 69943
Avahi laniger FMNH 5654 Leontopithecus rosalia FMNH 46164
Daubentonia madagascarensis FMNH 15529 Callicebus brunneus FMNH 84221
Tarsius bancanus FMNH 76856 " caligatus FMNH 88858
" syrichta FMNH 56756 " cupreus FMNH 25336
Aotus nigriceps FMNH 84226 " donacophilus FMNH 121650
" infulatus FMNH 25347 " hoffmannsi FMNH 50862
" azarai FMNH 21410 " moloch FMNH 50872
" lemurinus FMNH 68860 Cebus albifrons FMNH 22193
" vociferans FMNH 70684 " apella FMNH 46180
" nancymaae FMNH 122766 " capucinus FMNH 69648
" miconax FMNH 25345 Saimiri boliviensis FMNH 78675
" scireus FMNH 87821
Cathemeral Pithecia pithecia FMNH 50883
Genus Species FMNH Cat # Chiropotes satanas FMNH 46179
Eulemur fulvus Cacajao calvus FMNH 88813
" macaco Alouatta seniculus FMNH 95493
" rubriventer Ateles Spp. FMNH 12727
Hapalemur griseus Lagothrix lagotricha FMNH 98050
Macaca arctoides FMNH 39160
" assamensis FMNH 38018
" fascicularis FMNH 33507
" mulatta FMNH 99669
Papio anubis FMNH 127798
Theropithecus gelada FMNH 27185
Cercocebus Spp. FMNH 165381
Chlorocebus aethiops FMNH 93621
Erythrocebus patas FMNH 51441
Cercopithecus diana FMNH 51517
Colobus guereza FMNH 60113
Presbytis obscura FMNH 105692
Pygathrix roxellana FMNH 31144
Nasalis larvatus FMNH 15517
Hylobates lar FMNH 99751
Pongo pygmaeus FMNH 153745
Gorilla gorilla FMNH
Pan troglodytes FMNH
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modified from original, tables and hypotheses excluded