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The chiropteran paratympanic organ.

Abstract: Variation in atmospheric pressure is a potential source of information that might be used by flying animals as the basis of a pressure altimeter and/ or meteorological forecasting. A putative atmospheric pressure receptor found in the avian middle ear, the paratympanic organ, has also been reported to occur in the middle ear of some bats. In that report, the paratympanic organ was of variable occurrence in the bat Pipistrellus pipistrellus and was not observed in five other species examined. My examination of the microanatomy of the middle ear of P. pipistrellus failed to confirm the previous report of a paratympanic organ in this species. 1 also did not observe a paratympanic organ in specimens of ten other bat species.

Key words: bat, paratympanic, pressure, middle ear

Introduction

A small sensory structure that develops in association with the hyomandibular cleft in vertebrate embryos (von Bartheld, 1990) is retained beyond early embryological development in only a few vertebrates (Simonetta, 1953). This embryonic structure persists throughout adult life as the spiracular organ in nonteleost fish (Wright, 1885) and the paratympanic organ in a few reptiles (Simonetta, 1953), most birds (Vitali, 1911) and perhaps one bat species (Vitali, 1924). The anatomy of the spiracular organ in nonteleost fish has been described (Wright, 1885; Barry and Boord, 1984; Barry et. al., 1988a) and appears to have a proprioceptive function that responds to movements of the hyomandibular-cranial joint (Barry et. al., 1988b). The reptilian paratympanic organ has received little study (Simonetta, 1953). The avian paratympanic organ has been described in great detail (Vitali, 1911; Vitali, 1912; Simonetta, 1953; Petrash et. al., 1983; Jorgensen, 1984; Giannessi and Pera, 1986; Giannessi, 1989; von Bartheld, 1994; Giannessi and Ruffoli, 1996) and functions in a manner that is consistent with the detection of atmospheric pressure (von Bartheld, 1994). Vitali (1924) reported the presence of a paratympanic organ in the bat Pipistrellus pipistrellus that was of variable occurrence and rudimentary in conformation compared with the paratympanic organ in birds. Only two of the six P pipistrellus examined were reported to have had a paratympanic organ. None of the specimens of Rhinolophus ferrumequini, Rhinolophus hipposideros, Nyctalus noctula, Vespertilio murinus and Plecotus auritus examined by Vitali (1924) were reported to have a paratympanic organ.

The occurrence of the paratympanic organ in bats is of interest because it has been suggested that several species of temperate, insectivorous bats can detect changes in atmospheric pressure (Paige, 1995; Scott and Vaughan, 1997). In these studies, the detection of atmospheric pressure was discussed in relation to the presumed function of the paratympanic organ as an atmospheric pressure detector. However, the report by Vitali (1924) does not support the common presence of the paratympanic organ in bats. In fact, an alternate mechanism for pressure detection by some mammals has been suggested by the presence of stretch receptors in the human tympanic membrane (Rockley and Hawke, 1992). The objective of this study was to reexamine P. pipistrellus for the presence of a paratympanic organ and also to increase the number of bat species surveyed for the presence of the paratympanic organ.

Methods

Adult specimens of 11 microchiropteran bat species were obtained and examined. Two specimens of P. pipistrellus that had been fixed by immersion in ethanol were obtained from collections at the American Museum of Natural History. A third P. pipistrellus specimen fixed by immersion in 4% paraformaldehyde was provided by D. H. Pauza, Kaunas, Lithuania. Four specimens each of Pipistrellus subflavus, Eptesicus fuscus, Myotis velifer and Tadarida brasiliensis were immersion fixed in 3% glutaraldehyde in phosphate buffered saline (PBS) overnight. The entire middle ear region of all specimens was removed by dissection under the microscope, rinsed in PBS, decalcified for seven days in 10% EDTA (pH 7), stained in 2% osmium tetroxide in PBS for 1 hour, dehydrated in alcohol and propylene oxide and embedded in Epon (Electron Microscopy Supplies). Serial sections 10 pm thick were taken from throughout the middle ear. Alternate sections were collected on gelatine coated slides and stained with 1% Toluidine Blue O in 1% Borax. Six other bat species were examined: Rhinolophus rouxi (n = 1), Pteronotus parnellii (n = 2), Pteronotus quadridens (n = 1), Natalus stramineus (n = 1), Eumops perotis (n = 1) and Leptonycteris sp (n = 1). These six species were provided as prepared slides of serial sections throughout the middle ear of bats that had been used in previous research (Henson, 1961). All slides were examined using a light microscope up to 1000X magnification.

Results

Table 1 lists all of the species of bats that were examined in this study as well as all of the bat species that were examined by Vitali (1924). I did not observe a paratympanic organ in any of the P. pipistrellus specimens I examined. I also did not observe a paratympanic organ in the specimens of P. subflavus, M. velifer, E. fuscus, T. brasiliensis, R. rouxi, P. parnellii, P. quadridens, N. stramineus, E. perotis and Leptonycteris sp. Discussion

The paratympanic organ does not appear to be a common anatomical feature in the middle ear of microchiropteran bats. The only reported occurrence of the paratympanic organ in a bat is in P. pipistrellus (Vitali, 1924) out of a combined total of 16 species examined. In that early report, the occurrence of the paratympanic organ was variable with it only being reported in 2 of 6 specimens. This current study was unable to confirm the earlier report since no paratympanic organ was observed in the three P. pipistrellus specimens examined. If Vitali (1924) was correct in reporting his observations, there are two possible explanations for the discrepancy in the observations. If the occurrence of the paratympanic organ in P. pipistrellus is variable, it may have simply not been in the specimens I examined. Alternatively, the discrepancy might be due to species confusion since P. pipistrellus has been recently discovered to exist as two separate cryptic species (Barratt et al., 1997). If only one of the two species has the paratympanic organ, it is possible that the specimens examined by Vitali (1924) contained some of each species and that my specimens were all of the species without a paratympanic organ. Further examination of known species samples would be necessary to resolve this issue.

Since some bats appear to be able to detect variation in atmospheric pressure (Paige, 1995, Scott and Vaughan, 1997), there must be an alternative pressure detection mechanism other than the paratympanic organ. One alternate atmospheric pressure detection mechanism that has been proposed for mammals is in the function of stretch receptors in the tympanic membrane (Rockley and Hawke, 1992). If bats also have stretch receptors in their tympanic membranes, it is possible that bats detect variation in atmospheric pressure using this mechanism.
Table 1. Bat species examined for the occurrence of the
paratympanic organ.

Species # examined paratympanic
 organ

from Vitali (1924)
P. pipistrellus 6 yes, in 2 of 6
R. ferrumequini 1 no
N. hipposideros 1 no
N. noctula 2 no
V. murinus 1 no
P. auritus 1 no
This study
P. pipistrellus 3 no
P. subflavus 4 no
E. fuscus 4 no
M. velifer 4 no
T. brasiliensis 4 no
R. rouxi 1 no
P. parnellii 2 no
P. quadridens 1 no
N. stramineus 1 no
E. perotis 1 no
Leptonycteris sp 1 no


References

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Barry, M. A., D. H. Hall and M. V. L. Bennet. 1988a. The elasmobranch spiracular organ. I. Morphological studies. J. Comp. Physiol. A.163:85-92.

Barry, M. A., R. White and M. V. L. Bennet. 1988b. The elasmobranch spiracular organ. II. Electrophysiological studies. J. Comp. Physiol. A. 163:93-98.

Giannessi, F. and L. Pera. 1986. The ultrastructure of the paratympanic organ in the domestic fowl (Gallus gallus domesticus). J. Anat. 147:191-199.

--. 1989. On the presence of reciprocal synapses in the paratympanicorgan of the chicken. Anat. Embryol. 180:175-178.

Giannessi, F. and R. Ruffoli. 1996. Fine structure of the afferent synapses in the paratympanic organ of the chicken, with special reference to the synaptic bodies. Ann. Anat. 178:127-131.

Henson, O. W. 1961. Somemorphological and functional aspects of certain structures in the middle ear in bats and insectivores. Univ. Ks. Sci. Bull. 3:151-255.

Jorgensen, J. M. 1984. Fine structure of the paratympanic organ in the avian middle ear. Acta Zool. 65:89-94.

Paige, K. N. 1995. Bats and barometric pressure: conserving limited energy and tracking insects from the roost. Func. Ecol. 9:463-467.

Petrash, E. W., K. H. Andres, M. Von During and J. D. Delius. 1983. Morphologische aspekte des Vitali-Organs bei der taube. Anat. Anz. 153:288

Rockley, T. J. and W. M. Hawk. 1992. The middle ear as a baroreceptor. Acta Otolaryngology. 112:816-823.

Scott, M. G. and G. L. Vaughan. 1997. Induced atmospheric pressure changes elicit spontaneous responses in bats. J. Tenn. Acad. Sci. 72:42-44.

Simonetta, A. 1953. L'organo di senso dello spiracolo e l'organo paratimpanico nell sistematica dei Vertebrati. Arch. Ital. Anat. Embryol. 58:266-294.

Vitali, G. 1911. Di un intressante derivato della prima fessurabranchialenelpassero. Anat. Anz. 39:219-224.

--. 1912. Di un intressante derivato dell'ectoderma della prima fessura branchiale nel passero: un organo nervoso di senso nell'orecchio medio degli ucceli. Anat. Anz. 40:631-639.

--. 1924. Il comportamento dell'organo della prima fessura branchiale, negli anfibi, nei rettili, nei mammiferi. Ric. di Morf. 4:191-220.

von Bartheld, C. S. 1990. Development and innervation of the paratympanic organ (vitali organ) in chick embryos. Brain Behav. Evol. 35:1-15.

--. 1994. Functional morphology of the paratympanic organ in the middle ear of birds. Brain Behav. Evol. 44:61-73.

Wright, R. R.1885. On the hyomandibular clefts and pseudobranchs of Lepidosterous and Amia. J. Anat. Physiol. 19:476-499.

Michael G. Scott

Department of Agriculture and Natural Sciences

Lincoln University

Jefferson City, MO 65102

(573) 681-5120

scottm@lincolnu.edu
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Author:Scott, Michael G.
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Date:Jan 1, 2003
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