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, 219 (2), 229-42

The Development of the Olfactory Organs in Newly Hatched Monotremes and Neonate Marsupials

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The Development of the Olfactory Organs in Newly Hatched Monotremes and Neonate Marsupials

Nanette Yvette Schneider. J Anat.

Abstract

Olfactory cues are thought to play a crucial role in the detection of the milk source at birth in mammals. It has been shown that a marsupial, the tammar wallaby, can detect olfactory cues from its mother's pouch at birth. This study investigates whether the main olfactory and accessory olfactory system are similarly well developed in other marsupials and monotremes at birth/hatching as in the tammar. Sections of the head of various marsupial and two monotreme species were investigated by light microscopy. Both olfactory systems were less well developed in the kowari and Eastern quoll. No olfactory or vomeronasal or terminal nerves could be observed; the main olfactory bulb (MOB) had only two layers while no accessory olfactory bulb or ganglion terminale were visible. All other investigated marsupials and monotremes showed further developed olfactory systems with olfactory, vomeronasal and terminal nerves, a three-layered MOB, and in the marsupials a prominent ganglion terminale. The main olfactory system was further developed than the accessory olfactory system in all species investigated. The olfactory systems were the least developed in species in which the mother's birth position removed most of the difficulty in reaching the teat, placing the neonate directly in the pouch. In monotremes they were the furthest developed as Bowman glands were found underlying the main olfactory epithelium. This may reflect the need to locate the milk field each time they drink as they cannot permanently attach to it, unlike therian mammals. While it still needs to be determined how an odour signal could be further processed in the brain, this study suggests that marsupials and monotremes possess well enough developed olfactory systems to be able to detect an odour cue from the mammary area at birth/hatching. It is therefore likely that neonate marsupials and newly hatched monotremes find their way to the milk source using olfactory cues, as has been previously suggested for the marsupial tammar wallaby, rabbits, rats and other eutherians.

Figures

Fig. 1
Fig. 1
Development of newly hatched monotreme and neonate marsupials. The short-beaked echidna (a) has strongly developed forelimbs, while its hindlimbs are more paddle-like with slight digital rays. An egg tooth (ET) and a caruncle (C), typical for the newly hatched monotremes, are visible at the tip of the snoot. It helps the monotreme to open the egg. Parts of the foetal membranes (FM) are still attached to the abdomen. All neonate marsupials have stronger developed forelimbs than hindlimbs: (b) Virginia opossum; (c) grey short-tailed opossum; (d) Eastern quoll; (e) koala; (f) brushtail possum; and (g) Southern brown bandicoot. The forming ear is visible in the Virginia opossum, the koala, the brushtail possum and the Southern brown bandicoot. The pigment epithelium of the eye is shining through the skin in the short-beaked echidna, grey short-tailed opossum, koala, brushtail possum and the Southern brown bandicoot.
Fig. 2
Fig. 2
Measurements of the MOE, the VNO length and vomeronasal receptor epithelium height. (a) On the top is described how the height of the MOE was measured in both nasal cavities in the middle of the nasal cavity roof at the area of the caudal end of VNO in each cavity. In transverse and sagittal sections the appearance of the olfactory bulb in the section was used as a marker to determine the section in which the MOE was measured. (b) The height of the vomeronasal receptor epithelium was measured in the middle of the medial epithelium (which is where the vomeronasal receptor epithelium is mostly situated in mammals) in the middle of the VNO duct in coronal and transverse sections. (c) The length of the VNO was measured directly on one section in sagittal and transverse sections as shown here.
Fig. 3
Fig. 3
Development of the rhinarium. The echidna (not shown) does not possess an oral shield as found in some marsupial neonates. The Virginia opossum (a) and grey short-tailed opossum (b,c) show an oral shield-like rhinarium structure with slightly visible lib faults. In comparison to this the northern quoll (d) has a well-developed oral shield in which no difference is apparent between the upper and lower mandible. The oral shield is vestigial in the koala (e) and simple in the brushtail possum (f) and Southern brown bandicoot (g). LF, lip fold; N, naris; SM, sulcus medianus; T, tongue.
Fig. 4
Fig. 4
Development of the main olfactory epithelium (MOE). While the MOE of the newly hatched platypus (A) shows already Bowman glands (marked by arrows; close-up on right side), the red-necked pademelon (B) as well as all the other investigated marsupial neonates showed no Bowman glands. VNO, vomeronasal organ. Scale of both photos is 400 μm. Staining: Azan and H & E.
Fig. 5
Fig. 5
The development of the olfactory bulb. The majority of investigated neonates’/hatchling's MOBs show three different cell layers, the olfactory nerve layer (ONL), neuroepithelium (NE) and a layer in between the two long-nosed bandicoot (C), Southern brown bandicoot (D), tammar wallaby (E), red-necked pademelon (F), brushtail possum (G), koala (H), grey short-tailed opossum (I), platypus (J)]. In the section of the neonate koala these are difficult to distinguish but they are visible in the better-conserved tissue of the two koala embryos, which are not shown in this figure. The section of the kowari (A) and Eastern quoll (B) do only show two layers. In all species beside the kowari (A), Eastern quoll (B) and the platypus (J) was a ganglion terminale (GT) found. (A) Transverse section; (B–H) coronal sections. Staining: H & E and Azan. Scale bar: 200μm. OV, olfactory ventricle.
Fig. 6
Fig. 6
The development of the vomeronasal organ (VNO). The transverse section shows the VNOs of the kowari (A). The cross-sections show the VNOs of the Eastern quoll (B), long-nosed bandicoot (C), Southern brown bandicoot (D), tammar wallaby (E), red-necked pademelon (F), brushtail possum (G), koala (H), grey short-tailed opossum (I) and platypus (J). Staining: Mallory's trichrome stain H & E and Azan. Scale bar: 200 μm.

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