Cargando…

The Tongue in Three Species of Lemurs: Flower and Nectar Feeding Adaptations

SIMPLE SUMMARY: Comparative studies of primate gustatory anatomy are sparse and incomplete. Here, we compare both the macro and micro anatomy of the tongue in three lemurid species. We included two non-destructive nectar-feeders, Varecia variegata and Eulemur macaco, and one destructive flower feede...

Descripción completa

Detalles Bibliográficos
Autores principales: Pastor, Juan Francisco, Muchlinski, Magdalena Natalia, Potau, Josep Maria, Casado, Aroa, García-Mesa, Yolanda, Vega, Jose Antonio, Cabo, Roberto
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8532830/
https://www.ncbi.nlm.nih.gov/pubmed/34679832
http://dx.doi.org/10.3390/ani11102811
_version_ 1784587163480883200
author Pastor, Juan Francisco
Muchlinski, Magdalena Natalia
Potau, Josep Maria
Casado, Aroa
García-Mesa, Yolanda
Vega, Jose Antonio
Cabo, Roberto
author_facet Pastor, Juan Francisco
Muchlinski, Magdalena Natalia
Potau, Josep Maria
Casado, Aroa
García-Mesa, Yolanda
Vega, Jose Antonio
Cabo, Roberto
author_sort Pastor, Juan Francisco
collection PubMed
description SIMPLE SUMMARY: Comparative studies of primate gustatory anatomy are sparse and incomplete. Here, we compare both the macro and micro anatomy of the tongue in three lemurid species. We included two non-destructive nectar-feeders, Varecia variegata and Eulemur macaco, and one destructive flower feeder, Lemur catta. To study the tongue’s structure, we used direct observation together with different microscopy techniques, ranging from optical microscopy to electronic microscopy. We found differences in the size, shape, and distribution of the tongue’s papillae. Most notably, there are large distinct papillae present at the tip of the tongue in nectar-feeding species. In addition, histological images of the ventro-apical portion of the tongue show that tongue houses an encapsulated structure in all species studied. The non-destructive flower-feeding species share similar tongue and sublingua anatomy, suggesting that the observed features may be adaptive for flower feeding. These features were not observed in the destructive flower feeder, Lemur catta. ABSTRACT: The mobility of the primate tongue allows for the manipulation of food, but, in addition, houses both general sensory afferents and special sensory end organs. Taste buds can be found across the tongue, but the ones found within the fungiform papillae on the anterior two thirds of the tongue are the first gustatory structures to come into contact with food, and are critical in making food ingestion decisions. Comparative studies of both the macro and micro anatomy in primates are sparse and incomplete, yet there is evidence that gustatory adaptation exists in several primate taxa. One is the distally feathered tongues observed in non-destructive nectar feeders, such as Eulemur rubriventer. We compare both the macro and micro anatomy of three lemurid species who died of natural causes in captivity. We included the following two non-destructive nectar feeders: Varecia variegata and Eulemur macaco, and the following destructive flower feeder: Lemur catta. Strepsirrhines and tarsiers are unique among primates, because they possess a sublingua, which is an anatomical structure that is located below the tongue. We include a microanatomical description of both the tongue and sublingua, which were accomplished using hematoxylin–eosin and Masson trichrome stains, and scanning electron microscopy. We found differences in the size, shape, and distribution of fungiform papillae, and differences in the morphology of conical papillae surrounding the circumvallate ones in all three species. Most notably, large distinct papillae were present at the tip of the tongue in nectar-feeding species. In addition, histological images of the ventro-apical portion of the tongue displayed that it houses an encapsulated structure, but only in Lemur catta case such structure presents cartilage inside. The presence of an encapsulated structure, coupled with the shared morphological traits associated with the sublingua and the tongue tip in Varecia variegata and Eulemur macaco, point to possible feeding adaptations that facilitate non-destructive flower feeding in these two lemurids.
format Online
Article
Text
id pubmed-8532830
institution National Center for Biotechnology Information
language English
publishDate 2021
publisher MDPI
record_format MEDLINE/PubMed
spelling pubmed-85328302021-10-23 The Tongue in Three Species of Lemurs: Flower and Nectar Feeding Adaptations Pastor, Juan Francisco Muchlinski, Magdalena Natalia Potau, Josep Maria Casado, Aroa García-Mesa, Yolanda Vega, Jose Antonio Cabo, Roberto Animals (Basel) Article SIMPLE SUMMARY: Comparative studies of primate gustatory anatomy are sparse and incomplete. Here, we compare both the macro and micro anatomy of the tongue in three lemurid species. We included two non-destructive nectar-feeders, Varecia variegata and Eulemur macaco, and one destructive flower feeder, Lemur catta. To study the tongue’s structure, we used direct observation together with different microscopy techniques, ranging from optical microscopy to electronic microscopy. We found differences in the size, shape, and distribution of the tongue’s papillae. Most notably, there are large distinct papillae present at the tip of the tongue in nectar-feeding species. In addition, histological images of the ventro-apical portion of the tongue show that tongue houses an encapsulated structure in all species studied. The non-destructive flower-feeding species share similar tongue and sublingua anatomy, suggesting that the observed features may be adaptive for flower feeding. These features were not observed in the destructive flower feeder, Lemur catta. ABSTRACT: The mobility of the primate tongue allows for the manipulation of food, but, in addition, houses both general sensory afferents and special sensory end organs. Taste buds can be found across the tongue, but the ones found within the fungiform papillae on the anterior two thirds of the tongue are the first gustatory structures to come into contact with food, and are critical in making food ingestion decisions. Comparative studies of both the macro and micro anatomy in primates are sparse and incomplete, yet there is evidence that gustatory adaptation exists in several primate taxa. One is the distally feathered tongues observed in non-destructive nectar feeders, such as Eulemur rubriventer. We compare both the macro and micro anatomy of three lemurid species who died of natural causes in captivity. We included the following two non-destructive nectar feeders: Varecia variegata and Eulemur macaco, and the following destructive flower feeder: Lemur catta. Strepsirrhines and tarsiers are unique among primates, because they possess a sublingua, which is an anatomical structure that is located below the tongue. We include a microanatomical description of both the tongue and sublingua, which were accomplished using hematoxylin–eosin and Masson trichrome stains, and scanning electron microscopy. We found differences in the size, shape, and distribution of fungiform papillae, and differences in the morphology of conical papillae surrounding the circumvallate ones in all three species. Most notably, large distinct papillae were present at the tip of the tongue in nectar-feeding species. In addition, histological images of the ventro-apical portion of the tongue displayed that it houses an encapsulated structure, but only in Lemur catta case such structure presents cartilage inside. The presence of an encapsulated structure, coupled with the shared morphological traits associated with the sublingua and the tongue tip in Varecia variegata and Eulemur macaco, point to possible feeding adaptations that facilitate non-destructive flower feeding in these two lemurids. MDPI 2021-09-27 /pmc/articles/PMC8532830/ /pubmed/34679832 http://dx.doi.org/10.3390/ani11102811 Text en © 2021 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Pastor, Juan Francisco
Muchlinski, Magdalena Natalia
Potau, Josep Maria
Casado, Aroa
García-Mesa, Yolanda
Vega, Jose Antonio
Cabo, Roberto
The Tongue in Three Species of Lemurs: Flower and Nectar Feeding Adaptations
title The Tongue in Three Species of Lemurs: Flower and Nectar Feeding Adaptations
title_full The Tongue in Three Species of Lemurs: Flower and Nectar Feeding Adaptations
title_fullStr The Tongue in Three Species of Lemurs: Flower and Nectar Feeding Adaptations
title_full_unstemmed The Tongue in Three Species of Lemurs: Flower and Nectar Feeding Adaptations
title_short The Tongue in Three Species of Lemurs: Flower and Nectar Feeding Adaptations
title_sort tongue in three species of lemurs: flower and nectar feeding adaptations
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8532830/
https://www.ncbi.nlm.nih.gov/pubmed/34679832
http://dx.doi.org/10.3390/ani11102811
work_keys_str_mv AT pastorjuanfrancisco thetongueinthreespeciesoflemursflowerandnectarfeedingadaptations
AT muchlinskimagdalenanatalia thetongueinthreespeciesoflemursflowerandnectarfeedingadaptations
AT potaujosepmaria thetongueinthreespeciesoflemursflowerandnectarfeedingadaptations
AT casadoaroa thetongueinthreespeciesoflemursflowerandnectarfeedingadaptations
AT garciamesayolanda thetongueinthreespeciesoflemursflowerandnectarfeedingadaptations
AT vegajoseantonio thetongueinthreespeciesoflemursflowerandnectarfeedingadaptations
AT caboroberto thetongueinthreespeciesoflemursflowerandnectarfeedingadaptations
AT pastorjuanfrancisco tongueinthreespeciesoflemursflowerandnectarfeedingadaptations
AT muchlinskimagdalenanatalia tongueinthreespeciesoflemursflowerandnectarfeedingadaptations
AT potaujosepmaria tongueinthreespeciesoflemursflowerandnectarfeedingadaptations
AT casadoaroa tongueinthreespeciesoflemursflowerandnectarfeedingadaptations
AT garciamesayolanda tongueinthreespeciesoflemursflowerandnectarfeedingadaptations
AT vegajoseantonio tongueinthreespeciesoflemursflowerandnectarfeedingadaptations
AT caboroberto tongueinthreespeciesoflemursflowerandnectarfeedingadaptations