Susan J. Rehorek

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.

The Orbitofacial Glands of Bats: An Investigation of the Potential Correlation of Gland Structure with Social Organization

The facial glands of bats are modified skin glands, whereas there are up to three different orbital glands: Harderian, lacrimal, and Meibomian glands. Scattered studies have described the lacrimal and Meibomian glands in a handful of bat species, but there is as yet no description of a Harderian gland in bats. In this study we examined serial sections of orbitofacial glands in eight families of bats. Much variation amongst species was observed, with few phylogenetic patterns emerging. Enlarged facial glands, either sudoriparous (five genera) or sebaceous (vespertilionids only) were observed. Meibomian and lacrimal glands were present in most species examined (except Antrozous), though the relative level of development varied. Two types of anterior orbital glands were distinguished: the Harderian gland (tubulo‐acinar: observed in Rousettus, Atribeus, Desmodus and Miniopterus) and caruncular (sebaceous: observed in Eptesicus and Dieamus). The relative development of the nasolacrimal duct and the vomeronasal organ did not appear to be correlated with the development of any of the exocrine glands examined. There does, however, appear to be a correlation between the presence of at least one well developed exocrine gland and the level of communality and known olfactory acuity, best documented in Artibeus, Desmodus, and Miniopterus. Anat Rec 293:1433–1448, 2010.

A re-examination and re-evaluation of salamander orbital glands

The amphibian integument contains numerous multicellular glands. Although two of these, the nasolabial and orbital glands and the associated nasolacrimal duct (NLD), have historically received considerable attention, interpretation of the original observations can be problematic in the context of current literature. Salamanders, in particular, are frequently regarded as at least indicative of aspects of the morphology of the common ancestor to all extant tetrapods; hence, an understanding of these glands in salamanders might prove to be informative about their evolution. For this study, the orbitonasal region of salamanders from three families was histologically examined. Three themes emerged: (1) examination of the effect of phylogeny on the nasolabial gland and NLD revealed a combination of features that may be unique to plethodontid salamanders, and may be correlated to their nose‐tapping behavior by which substances are moved into the vomeronasal organ; (2) ecology appears to impact the relative development of the orbital glands, but not necessarily the nasolabial gland, with smaller glands being present in the aquatic species; (3) the nomenclature of the salamander orbital gland remains problematic, especially in light of comparative studies, as several alternate possibilities are viable. From this nomenclatural conundrum, however, it could be concluded that there may be a global pattern in the location of tetrapod orbital gland development. Molecular questions in terms of ontogeny and genetic homology affect the nature of the debate on orbital gland nomenclature. These observations suggest that rather than reflecting an ancestral condition, salamanders may instead represent a case of specialized, convergent evolution. Anat Rec, 296:1789–1796, 2013.

Membranous Support for Eyes of Strepsirrhine Primates and Fruit Bats

Living primates have relatively large eyes and support orbital tissues with a postorbital bar (POB) and/or septum. Some mammals with large eyes lack a POB, and presumably rely on soft tissues. Here, we examined the orbits of four species of strepsirrhine primates (Galagidae, Cheirogaleidae) and three species of fruit bats (Pteropodidae). Microdissection and light microscopy were employed to identify support structures of the orbit. In bats and primates, there are two layers of fascial sheets that border the eye laterally. The outer membrane is the most superficial layer of deep fascia, and has connections to the POB in primates. In fruit bats, which lacked a POB or analogous ligament, the deep fascia is reinforced by transverse ligaments. Bats and primates have a deeper membrane supporting the eye, identified as the periorbita (PA) based on the presence of elastic fibers and smooth muscle. The PA merges with periostea deep within the orbit, but has no periosteal attachment to the POB of primates. These findings demonstrate that relatively big eyes can be supported primarily with fibrous connective tissues as well as the PA, in absence of a POB or ligament. The well‐developed smooth muscle component within the PA of fruit bats likely helps to protrude the eye, maintaining a more convergent eye orientation, with greater overlap of the visual fields. The possibility should be considered that early euprimates, and even stem primates that may have lacked a POB, also had more convergent eyes than indicated by osseous measurements of orbital orientation. Anat Rec, 299:1690–1703, 2016.

Is It or Isn't It? A Reexamination of the Anterior Orbital Glands of the Fat-Tailed Dunnart Sminthopsis Crassicaudata (Dasyuridae: Marsupiala) and a Reevaluation of Definitions for the Harderian Gland

The anterior orbital glands of tetrapods, which include the Harderian and nictitans glands, can usually be differentiated either anatomically (nictitans gland is more anterior) or histochemically (Harderian gland secretes lipids). However, conflicting statements exist in the literature about the presence and identity of these glands. Two previous studies on Sminthopsis crassicaudata (Dasyuridae: Marsupiala) either failed to note any anterior ocular glands or used no histochemical analyses. This study reexamined the structure of the anterior orbital glands of S. crassicaudata. Histological, histochemical, and ultrastructural examination revealed three glandular units: two of which are located superficially in the nictitating membrane, the third lying deeper in the connective tissue. The ducts of these three glandular units all open onto the corneal aspect of the nictitating membrane. These cells contain mainly serous granules with sparse intracellular lipid droplets. The nomenclature of these structures depends upon the definition used. According to the anatomical definition, S. crassicaudata has two glands: anteriorly the nictitans and posteriorly the Harderian gland. In contrast, if the histochemical definition is used, there is only one gland, but its precise identity cannot be confirmed until the role of the lipid droplets is established. Moreover, the histochemical definition poses additional problems with respect to the mechanism of secretion, multiple secretions, and glandular plasticity. Finally, the unitary definition identifies one deeply subdivided gland with an anterior and a posterior lobe in S. crassicaudata. This last definition is broad enough to accommodate a wide level of anatomical variation in the anterior ocular glands of tetrapods. Anat Rec 293:1449–1454, 2010.

Early development and differentiation of the Laysan albatross (Phoebastria immutabilis (Rothschild, 1893): Procellariiformes)

Bird incubation is subdivided into two phases: differentiation (embryonic phase) and growth (fetal phase). Most birds have a relatively short incubation period (20–30 days) with the phase transition occurring midway through the incubation period. The Laysan albatross (Phoebastris immutabilis) is a large pelagic bird with a long incubation period. The purpose of this study was to document the differentiation phase with the aim of ascertaining the impact of a lengthened incubation on embryonic development. Eighty‐two previously collected albatross embryos were examined, measured, and staged. The albatross was found to develop more slowly than smaller birds, with a rate similar to other long‐incubating birds. Legs and wings grow at similar rates but exhibit variation in growth among their anatomical components. While the albatross embryos shared some morphological stages with chickens, they were more similar to ducks and pelicans. Special features of the albatross not shared with the Gallianserae (chickens and ducks) included an alligator‐like curved tail, narial tubes, and a cloacal bulge. Further examination of other larger pelagic birds with long incubation periods are needed to determine the uniqueness of the Laysan albatross embryonic development. Although much embryonic phase growth was documented in the postnatal period, little is known about the later, fetal phase in Laysan albatross. Future studies should involve examination of later (post day 32) fetuses. J. Morphol. 277:1231–1249, 2016.

Development of the nasolacrimal apparatus in the Mongolian gerbil (Meriones unguiculatus), with notes on network topology and function

The nasolacrimal apparatus (NLA) is a multicomponent functional system comprised of multiple orbital glands (up to four larger multicellular exocrine structures), a nasal chemosensory structure (vomeronasal organ: VNO), and a connecting duct (nasolacrimal duct: NLD). Although this system has been described in all tetrapod vertebrate lineages, albeit not always with all three main components present, considerably less is known about its ontogeny. The Mongolian gerbil (Meriones unguiculatus) is a common lab rodent in which the individual components of the adult NLA have been well studied, but as yet nothing is known about the ontogeny of the NLA. In this study, serial sections of 15 fetal and three adult Mongolian gerbil heads show that the development of the NLA falls into three fetal stages: inception (origin of all features), elongation (lengthening of all features), and expansion (widening of all features). No postnatal or juvenile specimens were observed in this study, but considerable growth evidently occurs before the final adult condition is reached. The development of the orbital glands and the VNO in the Mongolian gerbil is largely consistent with those in other mammals, despite a slight nomenclatural conundrum for the anterior orbital glands. However, the Mongolian gerbil NLD follows a more circuitous route than in other tetrapods, due mainly to the convoluted arrangement of the narial cartilages, the development of a pair of enlarged incisors as well as an enlarged infraorbital foramen. The impact of these associated features on the ontogeny and phylogeny of the NLA could be examined through the approach of network science. This approach allows for the incorporation of adaptations to specific lifestyles as potential explanations for the variation observed in the NLA across different tetrapod clades. J. Morphol. 276:1005–1024, 2015.

Histology of melanic flank and opercular color pattern elements in the firemouth cichlid, Thorichthys meeki

Dark melanic color pattern elements, such as bars, stripes, and spots, are common in the skin of fishes, and result from the differential distribution and activity of melanin‐containing chromatophores (melanophores). We determined the histological basis of two melanic color pattern elements in the integument of the Firemouth Cichlid, Thorichthys meeki. Vertical bars on the flanks were formed by three layers of dermal melanophores, whereas opercular spots were formed by four layers (two lateral and two medial) in the integument surrounding the opercular bones. Pretreatment of opercular tissue with potassium and sodium salts effectively concentrated or dispersed intracellular melanosomes. Regional differences in epidermal structure, scale distribution, and connective tissues were also identified. J. Morphol. 2013.

Testing the orbital lubrication hypothesis: the Harderian glands in burrowing skinks (Reptilia: Squamata)

The Harderian gland is an orbital gland thought to be a source of corneal lubricant, supplementary to the other orbital glands. This study investigated the possible role of skink Harderian glands in corneal lubrication. It was hypothesized that if these glands play a role in corneal lubrication, then the structure of these glands would be affected by structural orbital modifications. We examined the Harderian and lacrimal glands of five species of Australian skinks (Lygosominae), two of which possessed orbital modifications in the form of a transparent immoveable eyelid (spectacle) and skull reduction. All species possessed well-developed posterior lacrimal glands, but no anterior lacrimal glands. Anatomically, the Harderian glands were smaller in the burrowing species relative to the nonburrowing species. No other obvious species-specific differences were observed. The absence of any differentiation at the microscopic level suggests that although there is some change in the relative amount of secretant p...

Ontogeny of the orbital glands and their environs in the Pantropical Spotted Dolphin (Stenella attenuata: Delphinidae)

The nasolacrimal duct (NLD) connects the orbital (often associated with the Deep Anterior Orbital gland: DAOG, a.k.a. Harderian gland) and nasal regions in many tetrapods. Adult cetaceans are usually said to lack an NLD, and there is little agreement in the literature concerning the identity of their orbital glands, which may reflect conflicting definitions rather than taxonomic variation. In this study, we examined an embryological series of the pantropical spotted dolphin (Stenella attenuata), and report numerous divergences from other tetrapods. Underdeveloped eyelids and a few ventral orbital glands are present by late Stage (S) 17. By S 19, circumorbital conjunctival glands are present. In S 20, these conjunctival glands have proliferated, eyelids (and scattered palpebral glands) have formed, and a duct similar to the NLD has appeared. Subsequently, both the palpebral glands and the NLD are progressively reduced by S 22, even as the conjunctival glands exhibit regional growth. In most tetrapods examined, the ontogeny of the NLD follows a series of three stages: Inception of NLD, Connection of orbit and nasal cavity by the NLD and Ossification (i.e., formation of the bony canal surrounding the NLD, emerging into the orbit via the lacrimal foramen in the lacrimal bone). In contrast, the dolphin NLD originates at the same time as the lacrimal bone, and a lacrimal foramen fails to develop. The cetacean fossil record shows that a lacrimal foramen was present in the earliest ancestral amphibious, freshwater forms, but was soon lost as the lineage invaded the oceans. Anat Rec, 2017.