Intra-oropharyngeal food transport and swallowing in white-spotted bamboo sharks

Noraly M.M.E. van Meer, Hannah I. Weller, Armita R. Manafzadeh, Elska B. Kaczmarek, Bradley Scott, Sander W.S. Gussekloo, Cheryl D. Wilga, Elizabeth L. Brainerd, Ariel L. Camp

Research output: Contribution to journalArticleAcademicpeer-review

Abstract


Despite the importance of intraoral food transport and swallowing, relatively few studies have examined the biomechanics of these behaviors in non-tetrapods, which lack a muscular tongue. Studies show that elasmobranch and teleost fishes generate water currents as a ‘hydrodynamic tongue’ that presumably transports food towards and into the esophagus. However, it remains largely unknown how specific musculoskeletal motions during transport correspond to food motion. Previous studies of white-spotted bamboo sharks (Chiloscyllium plagiosum) hypothesized that motions of the hyoid, branchial arches and pectoral girdle, generate caudal motion of the food through the long oropharynx of modern sharks. To test these hypotheses, we measured food and cartilage motion with XROMM during intra-oropharyngeal transport and swallowing (N=3 individuals, 2–3 trials per individual). After entering the mouth, food does not move smoothly toward the esophagus, but rather moves in distinct steps with relatively little retrograde motion. Caudal food motion coincides with hyoid elevation and a closed mouth, supporting earlier studies showing that hyoid motion contributes to intra-oropharyngeal food transport by creating caudally directed water currents. Little correspondence between pectoral girdle and food motion was found, indicating minimal contribution of pectoral girdle motion. Transport speed was fast as food entered the mouth, slower and step-wise through the pharyngeal region and then fast again as it entered the esophagus. The food's static periods in the step-wise motion and its high velocity during swallowing could not be explained by hyoid or girdle motion, suggesting these sharks may also use the branchial arches for intra-oropharyngeal transport and swallowing
Original languageEnglish
Article numberjeb201426
Number of pages9
JournalJournal of Experimental Biology
Volume2019
Issue number222
DOIs
Publication statusPublished - 22 Nov 2019

Fingerprint

Chiloscyllium
food transport
Sharks
bamboo
Deglutition
shark
esophagus
Food
mouth
food
water currents
tongue
sharks
Chiloscyllium plagiosum
arch
cartilage
hydrodynamics
Esophagus
Branchial Region
Mouth

Cite this

van Meer, Noraly M.M.E. ; Weller, Hannah I. ; Manafzadeh, Armita R. ; Kaczmarek, Elska B. ; Scott, Bradley ; Gussekloo, Sander W.S. ; Wilga, Cheryl D. ; Brainerd, Elizabeth L. ; Camp, Ariel L. / Intra-oropharyngeal food transport and swallowing in white-spotted bamboo sharks. In: Journal of Experimental Biology. 2019 ; Vol. 2019, No. 222.
@article{7f19f0e2fda541e59854bcd40f77b30a,
title = "Intra-oropharyngeal food transport and swallowing in white-spotted bamboo sharks",
abstract = "Despite the importance of intraoral food transport and swallowing, relatively few studies have examined the biomechanics of these behaviors in non-tetrapods, which lack a muscular tongue. Studies show that elasmobranch and teleost fishes generate water currents as a ‘hydrodynamic tongue’ that presumably transports food towards and into the esophagus. However, it remains largely unknown how specific musculoskeletal motions during transport correspond to food motion. Previous studies of white-spotted bamboo sharks (Chiloscyllium plagiosum) hypothesized that motions of the hyoid, branchial arches and pectoral girdle, generate caudal motion of the food through the long oropharynx of modern sharks. To test these hypotheses, we measured food and cartilage motion with XROMM during intra-oropharyngeal transport and swallowing (N=3 individuals, 2–3 trials per individual). After entering the mouth, food does not move smoothly toward the esophagus, but rather moves in distinct steps with relatively little retrograde motion. Caudal food motion coincides with hyoid elevation and a closed mouth, supporting earlier studies showing that hyoid motion contributes to intra-oropharyngeal food transport by creating caudally directed water currents. Little correspondence between pectoral girdle and food motion was found, indicating minimal contribution of pectoral girdle motion. Transport speed was fast as food entered the mouth, slower and step-wise through the pharyngeal region and then fast again as it entered the esophagus. The food's static periods in the step-wise motion and its high velocity during swallowing could not be explained by hyoid or girdle motion, suggesting these sharks may also use the branchial arches for intra-oropharyngeal transport and swallowing",
author = "{van Meer}, {Noraly M.M.E.} and Weller, {Hannah I.} and Manafzadeh, {Armita R.} and Kaczmarek, {Elska B.} and Bradley Scott and Gussekloo, {Sander W.S.} and Wilga, {Cheryl D.} and Brainerd, {Elizabeth L.} and Camp, {Ariel L.}",
year = "2019",
month = "11",
day = "22",
doi = "10.1242/jeb.201426",
language = "English",
volume = "2019",
journal = "Journal of Experimental Biology",
issn = "0022-0949",
publisher = "Company of Biologists",
number = "222",

}

van Meer, NMME, Weller, HI, Manafzadeh, AR, Kaczmarek, EB, Scott, B, Gussekloo, SWS, Wilga, CD, Brainerd, EL & Camp, AL 2019, 'Intra-oropharyngeal food transport and swallowing in white-spotted bamboo sharks', Journal of Experimental Biology, vol. 2019, no. 222, jeb201426. https://doi.org/10.1242/jeb.201426

Intra-oropharyngeal food transport and swallowing in white-spotted bamboo sharks. / van Meer, Noraly M.M.E.; Weller, Hannah I.; Manafzadeh, Armita R.; Kaczmarek, Elska B.; Scott, Bradley; Gussekloo, Sander W.S.; Wilga, Cheryl D.; Brainerd, Elizabeth L. ; Camp, Ariel L.

In: Journal of Experimental Biology, Vol. 2019, No. 222, jeb201426, 22.11.2019.

Research output: Contribution to journalArticleAcademicpeer-review

TY - JOUR

T1 - Intra-oropharyngeal food transport and swallowing in white-spotted bamboo sharks

AU - van Meer, Noraly M.M.E.

AU - Weller, Hannah I.

AU - Manafzadeh, Armita R.

AU - Kaczmarek, Elska B.

AU - Scott, Bradley

AU - Gussekloo, Sander W.S.

AU - Wilga, Cheryl D.

AU - Brainerd, Elizabeth L.

AU - Camp, Ariel L.

PY - 2019/11/22

Y1 - 2019/11/22

N2 - Despite the importance of intraoral food transport and swallowing, relatively few studies have examined the biomechanics of these behaviors in non-tetrapods, which lack a muscular tongue. Studies show that elasmobranch and teleost fishes generate water currents as a ‘hydrodynamic tongue’ that presumably transports food towards and into the esophagus. However, it remains largely unknown how specific musculoskeletal motions during transport correspond to food motion. Previous studies of white-spotted bamboo sharks (Chiloscyllium plagiosum) hypothesized that motions of the hyoid, branchial arches and pectoral girdle, generate caudal motion of the food through the long oropharynx of modern sharks. To test these hypotheses, we measured food and cartilage motion with XROMM during intra-oropharyngeal transport and swallowing (N=3 individuals, 2–3 trials per individual). After entering the mouth, food does not move smoothly toward the esophagus, but rather moves in distinct steps with relatively little retrograde motion. Caudal food motion coincides with hyoid elevation and a closed mouth, supporting earlier studies showing that hyoid motion contributes to intra-oropharyngeal food transport by creating caudally directed water currents. Little correspondence between pectoral girdle and food motion was found, indicating minimal contribution of pectoral girdle motion. Transport speed was fast as food entered the mouth, slower and step-wise through the pharyngeal region and then fast again as it entered the esophagus. The food's static periods in the step-wise motion and its high velocity during swallowing could not be explained by hyoid or girdle motion, suggesting these sharks may also use the branchial arches for intra-oropharyngeal transport and swallowing

AB - Despite the importance of intraoral food transport and swallowing, relatively few studies have examined the biomechanics of these behaviors in non-tetrapods, which lack a muscular tongue. Studies show that elasmobranch and teleost fishes generate water currents as a ‘hydrodynamic tongue’ that presumably transports food towards and into the esophagus. However, it remains largely unknown how specific musculoskeletal motions during transport correspond to food motion. Previous studies of white-spotted bamboo sharks (Chiloscyllium plagiosum) hypothesized that motions of the hyoid, branchial arches and pectoral girdle, generate caudal motion of the food through the long oropharynx of modern sharks. To test these hypotheses, we measured food and cartilage motion with XROMM during intra-oropharyngeal transport and swallowing (N=3 individuals, 2–3 trials per individual). After entering the mouth, food does not move smoothly toward the esophagus, but rather moves in distinct steps with relatively little retrograde motion. Caudal food motion coincides with hyoid elevation and a closed mouth, supporting earlier studies showing that hyoid motion contributes to intra-oropharyngeal food transport by creating caudally directed water currents. Little correspondence between pectoral girdle and food motion was found, indicating minimal contribution of pectoral girdle motion. Transport speed was fast as food entered the mouth, slower and step-wise through the pharyngeal region and then fast again as it entered the esophagus. The food's static periods in the step-wise motion and its high velocity during swallowing could not be explained by hyoid or girdle motion, suggesting these sharks may also use the branchial arches for intra-oropharyngeal transport and swallowing

U2 - 10.1242/jeb.201426

DO - 10.1242/jeb.201426

M3 - Article

VL - 2019

JO - Journal of Experimental Biology

JF - Journal of Experimental Biology

SN - 0022-0949

IS - 222

M1 - jeb201426

ER -