Magdalena N. Muchlinski

Causes and significance of variation in mammalian basal metabolism

Mammalian basal metabolic rates (BMR) increase with body mass, whichs explains approximately 95% of the variation in BMR. However, at a given mass, there remains a large amount of variation in BMR. While many researchers suggest that the overall scaling of BMR with body mass is due to physiological constraints, variation at a given body mass may provide clues as to how selection acts on BMR. Here, we examine this variation in BMR in a broad sample of mammals and we test the hypothesis that, across mammals, body composition explains differences in BMR at a given body mass. Variation in BMR is strongly correlated with variation in muscle mass, and both of these variables are correlated with latitude and ambient temperature. These results suggest that selection alters BMR in response to thermoregulatory pressures, and that selection uses muscle mass as a means to generate this variation.

Muscle Mass Scaling in Primates: An Energetic and Ecological Perspective

Body composition is known to vary dramatically among mammals, even in closely related species, yet this issue has never been systematically investigated. Here, we examine differences in muscle mass scaling among mammals, and explore how primate body composition compares to that of nonprimate mammals. We use a literature‐based sample of eutherian and metatherian mammals, and combine this with new dissection‐based data on muscularity in a variety of strepsirrhine primates and the haplorhine, Tarsius syrichta. Our results indicate an isometric scaling relationship between total muscle mass and total body mass across mammals. However, we documented substantial variation in muscularity in mammals (21–61% of total body mass), which can be seen both within and between taxonomic groups. We also found that primates are under‐muscled when compared to other mammals. This difference in body composition may in part reflect the functional consequences of arboreality, as arboreal species have significantly lower levels of muscularity than terrestrial species. Am. J. Primatol. 74:395‐407, 2012.

Ecological correlates of infraorbital foramen area in primates.

The infraorbital foramen (IOF) transmits the infraorbital nerve (ION) to specialized sensory cells (mechanoreceptors) in the maxillary region. The size of the IOF has been used in numerous paleoecological interpretations of the fossil record. However, these interpretations have been applied without an explicit analysis of the relationship between ecological variables and the IOF. ION and IOF cross-sectional area show a strong positive correlation. As a result, IOF area can be a proxy for ION area, and it is hypothesized that IOF area may be a good measure for maxillary somatosensory acuity. Differences in diet, substrate preference, and/or activity pattern have been shown to correlate with differences in maxillary somatosensory acuity among mammals. This study examines how IOF area covaries with different ecological variables. IOF area was measured for 89 primate species. Ecological profiles were also created for each species and used to evaluate interspecific variation in relative IOF area within each ecological category. The results show a significant relationship between relative IOF area and diet, but not substrate preference or activity pattern. Frugivores have significantly larger relative IOFs than either folivores or insectivores, but the relative IOFs of folivores and insectivores do not differ significantly from one another. These results partially support the hypothesis that maxillary mechanoreception is a critical sensory cue for primates within a feeding context. Results for this study suggest the IOF can be used as an informative character in some paleoecological interpretations of the primate fossil record.

Eye size at birth in prosimian primates: life history correlates and growth patterns.

Background Primates have large eyes relative to head size, which profoundly influence the ontogenetic emergence of facial form. However, growth of the primate eye is only understood in a narrow taxonomic perspective, with information biased toward anthropoids. Methodology/Principal Findings We measured eye and bony orbit size in perinatal prosimian primates (17 strepsirrhine taxa and Tarsius syrichta) to infer the extent of prenatal as compared to postnatal eye growth. In addition, multiple linear regression was used to detect relationships of relative eye and orbit diameter to life history variables. ANOVA was used to determine if eye size differed according to activity pattern. In most of the species, eye diameter at birth measures more than half of that for adults. Two exceptions include Nycticebus and Tarsius, in which more than half of eye diameter growth occurs postnatally. Ratios of neonate/adult eye and orbit diameters indicate prenatal growth of the eye is actually more rapid than that of the orbit. For example, mean neonatal transverse eye diameter is 57.5% of the adult value (excluding Nycticebus and Tarsius), compared to 50.8% for orbital diameter. If Nycticebus is excluded, relative gestation age has a significant positive correlation with relative eye diameter in strepsirrhines, explaining 59% of the variance in relative transverse eye diameter. No significant differences were found among species with different activity patterns. Conclusions/Significance The primate developmental strategy of relatively long gestations is probably tied to an extended period of neural development, and this principle appears to apply to eye growth as well. Our findings indicate that growth rates of the eye and bony orbit are disassociated, with eyes growing faster prenatally, and the growth rate of the bony orbit exceeding that of the eyes after birth. Some well-documented patterns of orbital morphology in adult primates, such as the enlarged orbits of nocturnal species, mainly emerge during postnatal development.

Mechanoreceptivity of prehensile tail skin varies between ateline and cebine primates

Prehensile tails evolved independently twice in primates: once in the ateline subfamily of platyrrhine primates and once in the genus Cebus. Structurally, the prehensile tails of atelines and Cebus share morphological features distinguishing them from nonprehensile tails (e.g., robust and strong caudal vertebrae, well developed lateral tail musculature, etc.). However, because of their independent evolutionary histories, the prehensile tails of atelines exhibit some differences from the Cebus prehensile tail. Ateline tails are relatively longer than those of Cebus, and they have less well‐developed extensor compartment musculature. However, perhaps the most obvious difference is the distinctive hairless friction pad on the ventrodistal surface of the ateline tail; the tail of Cebus is completely covered in hair. This study documents the presence of four epicritic histologic mechanoreceptors in the friction pad of atelines: Meissners corpuscles, Pacinian corpuscles, Ruffini corpuscles, and Merkel discs. Ruffini corpuscles and Merkel cells were also identified in the ventrodistal skin of the Cebus tail. However, Meissners and Pacinian corpuscles (not typically associated with hairy skin) were not found in Cebus. Cebus was also compared to its closest living sister taxon, nonprehensile‐tailed Saimiri, in which genus only Ruffini corpuscles are observed (no Merkel discs). The differences in mechanoreceptor type and morphology are attributed to the contrasting behavioral and tactile demands of the tail as it is used in posture and locomotion, which also distinguishes atelines from Cebus. Anat Rec,, 2011.

Evidence for dietary niche separation based on infraorbital foramen size variation among subfossil lemurs.

The size of the infraorbital foramen (IOF) has been used in drawing both phylogenetic and ecological inferences regarding fossil taxa. Within the order Primates, frugivores have relatively larger IOFs than folivores or insectivores. This study uses relative IOF size in lemurs to test prior trophic inferences for subfossil lemurs and to explore the pattern of variation within and across lemur families. The IOFs of individuals belonging to 12 extinct lemur species were measured and compared to those of extant Malagasy strepsirhines. Observations matched expectations drawn from more traditional approaches (e.g. dental morphology and microwear, stable isotope analysis) remarkably well. We confirm that extinct lemurs belonging to the families Megaladapidae and Palaeopropithecidae were predominantly folivorous and that species belonging to the genus Pachylemur (Lemuridae) were frugivores. Very high values for relative IOF area in Archaeolemur support frugivory but are also consistent with omnivory, as certain omnivores use facial touch cues while feeding. These results provide additional evidence that the IOF can be used as an informative osteological feature in both phylogenetic and paleoecological interpretations of the fossil record.

Behavioral and ecological consequences of sex-based differences in gustatory anatomy in Cebus apella.

Fungiform papillae (FPs) are the only gustatory structures on the anterior tongue. Taste buds (TBs), which are located in FPs, house taste receptors. Each TB has a taste pore (TP) by which tastants are transmitted. In humans, FP and TB densities correlate with taste sensitivity and food preferences. Females have higher FP densities than males in Homo, Pan, and Cebus. Homo, Pan, and Cebus also have larger brains, slower ontogenetic development, and higher maternal investment in offspring compared to most primates. An increase in maternal investment places intense pressure on females to 1) obtain high‐quality foods, and 2) detect potential toxins at low levels. This study examines sex differences in FPs and TPs (a TB surrogate) in 11 Cebus apella to test the hypothesis that higher FP density in females may be an adaptation specific to reproductive strategies of females. Tongues were imaged using an environmental scanning electron microscope; from these images FP surface area, FP density, TP count, and TP densities were calculated. We found that there were no significant differences between males and females in the number of TPs per FP. However, we did find that females do have larger FP surface areas and higher FP densities than males. The anatomical evidence indicates that females may have greater taste sensitivity than males because females have more FP than males. Future research on food preference and selection in Cebus is expected to show sex‐specific behaviors similar to those observed in Homo and Pan. Anat Rec,, 2011.

Dental maturation, eruption, and gingival emergence in the upper jaw of newborn primates.

In this report we provide data on dental eruption and tooth germ maturation at birth in a large sample constituting the broadest array of non‐human primates studied to date. Over 100 perinatal primates, obtained from natural captive deaths, were screened for characteristics indicating premature birth, and were subsequently studied using a combination of histology and micro‐CT. Results reveal one probable unifying characteristic of living primates: relatively advanced maturation of deciduous teeth and M1 at birth. Beyond this, there is great diversity in the status of tooth eruption and maturation (dental stage) in the newborn primate. Contrasting strategies in producing a masticatory battery are already apparent at birth in strepsirrhines and anthropoids. Results show that dental maturation and eruption schedules are potentially independently co‐opted as different strategies for attaining feeding independence. The most common strategy in strepsirrhines is accelerating eruption and the maturation of the permanent dentition, including replacement teeth. Anthropoids, with only few exceptions, accelerate mineralization of the deciduous teeth, while delaying development of all permanent teeth except M1. These results also show that no living primate resembles the altricial tree shrew (Tupaia) in dental development. Our preliminary observations suggest that ecological explanations, such as diet, provide an explanation for certain morphological variations at birth. These results confirm previous work on perinatal indriids indicating that these and other primates telegraph their feeding adaptations well before masticatory anatomy is functional. Quantitative analyses are required to decipher specific dietary and other influences on dental size and maturation in the newborn primate. Anat Rec, 298:2098–2131, 2015.

The vomeronasal organ of Lemur catta

The vomeronasal organ (VNO), also known as the Jacobsons organ, is a bilateral chemosensory organ found at the base of the nasal cavity specialized for the detection of higher‐molecular weight (non‐volatile) chemostimuli. It has been linked to pheromone detection. The VNO has been well studied in nocturnal lemurs and lorises, but poorly studied in diurnal/cathemeral species despite the large repertoire of olfactory behaviors noted in species such as Lemur catta. Here, the VNO and associated structures were studied microanatomically in one adult female and one adult male L. catta. Traditional and immunohistochemical procedures demonstrate the VNO epithelium consists of multiple rows of sensory neurons. Immunoreactivity to Growth‐associated protein 43 (GAP43) indicates the VNO is postnatally neurogenic. In volume, the VNO neuroepithelium scales similarly to palatal length compared to nocturnal strepsirrhines. Numerous taste buds present at the oral opening to the nasopalatine duct, with which the VNO communicates, provide an additional (or alternative) explanation for the flehmen behavior that has been observed in this species. The VNO of L. catta is shown to be microanatomically comparable to that of nocturnal strepsirrhines. Like nocturnal strepsirrhines, the VNO of L. catta may be functional in the reception of high‐molecular weight secretions. Am. J. Primatol. 77:229–238, 2015.

The interpretive power of infraorbital foramen area in making dietary inferences in extant apes.

The infraorbital foramen (IOF) is located below the orbit and transmits the sensory infraorbital nerve (ION) to mechanoreceptors located throughout the maxillary region. The size of the IOF correlates with the size of the ION; thus, the IOF appears to indicate relative touch sensitivity of maxillary region. In primates, IOF size correlates well with diet. Frugivores have relatively larger IOFs than folivores or insectivores because fruit handling/processing requires increased touch sensitivity. However, it is unknown if the IOF can be used to detect subtle dietary differences among closely related hominoid species. Hominoids are traditionally grouped into broad dietary categories, despite the fact that hominoid diets are remarkably diverse. This study examines whether relative IOF size is capable of differentiating among the dietary preferences of closely related species with overlapping, yet divergent diets. We measured IOF area in Hylobates lar, Symphalangus syndactulus, Pongo pygmaeus spp., Pan troglodytes, Gorilla gorilla, Gorilla beringei graueri, and Gorilla beringei beringei. We classified each species as a dedicated folivore, mixed folivore/frugivore, soft object frugivore, or hard object frugivore. The IOF is documented to be larger in more frugivorous species and smaller in more folivorous taxa. Interestingly, G.b. beringei, had the largest relative IOF of any gorilla, despite being a dedicated folivore. G.b. beringei does have unique food processing behavior that relies heavily on maxillary mechanoreception, thus this finding is not entirely unsupported behaviorally. The results of this study provide evidence that the IOF is an informative feature in interpretations of fossil apes. Anat Rec, 297:1377–1384, 2014.