ANATOMICAL, BEHAVIORAL, AND PHYSIOLOGICAL STUDIES

327 Pages·2012·9.87 MB·English

ELECTRORECEPriON IN THE flATFISH
(SUBCLASS HOLOCEPHALI):
ANATOMICAL, BEHAVIORAL, AND PHYSIOLOGICAL STUDIES
Thesis
.~
Presented to
The Faculty a£ the Department of Biology
San Jose State University
In Partial Fulfillment
of the Requirements far the Degree
Master of Arts
By
R. Douglas Fields
August, 1982
ACKNOWLEIDMENTS
These ex~eriments were com~leted in 1977 and 1978, and the
early draft of this thesis was com~leted by the summer of 1978.
However, since leaving Landing Marine Labs. , the process of
~loss
editing, and the final thesis has been frequently delayed
t~ing
by other commitments. I have been extremely fortunate to have had
persistent sup~ort from ·the members of my committee throughout
the protracted period of time that it has taken to finish this
project.
I thank Dr. Gregor Cailliet, my major advisor, for early
encouragement and continued guidance, and for his valuable scientific
and editorial instruction. Dr. Ann Hurley has been especially
helpful in the behavioral aspects of this research, and in the
statistical analysis of the data. Dr. David Lange, in his generous
manner, provided equipment and direction which made the neuro
physiological experiments possible. And finally, my sincere
gratitude to my wife, Melanie, who was always there to support and
share in the ex~eriments, from the first time the fish "did it"
to the completion of this project. Thanks to these, and all others
at Moss Landing and elsewhere who have helped me in their own
special ways to see the day when I finally put the period at
c~~
the end of this sentence.
ABSTRACT
Behavioral and neurophysiological experiments and anatomical
work indicate that the ampullar structures on the head of fish of
the subclass Holocephali are sense organs responsive to weak electric
fields, and are homologous to the ampullae of Lorenzini in elasmobranchs.
It is concluded that, as in elasmobranchs, these organs are used
to detect bioelectric and other natural electric phenomeP4 in the
environment.
In behavioral experiments, the ratfish colliei
~~£1~~
was conditioned in a ring-shaped aquarium to respond to the presence
of an electric field by reversing its direction of swimming. The
conditioning stimulus was generated by passing a 5Hz square wave
or DC current of 1 to 10 !-lA beb1een a bipolar electrode on the
floor of the aquarium. Under these conditions the fish perceived
electric fields as weak as 0.2 uv/cm.
The gross anatomy of the lateral line and the ampullar organs
t.-as studied, as as the peripheral distribution of the lateral
line and cranial nerves of H. colliei. The buccal, hyowandibular,
and superficial opthalmic branches of the anterior lateral line nerve
iv
were found to innervate the ampullar organs. Histological and
ultrastructural studies provide further evidence that the ampullar
organs are electroreceptive, and homologous to those of the elasmobranchs.
The ampullae contain ciliated sense cells located in an alveolate-
shaped epithelium, which communicates to the surface through a
jelly-filled tube. These sense cells synapse at their bases with
the afferent neurons of the anterior lateral line nerve, which
terminate in the medulla.
That the ampullar organs are electrosensory was confirmed by
direct recording from the afferent nerves of these receptors.
Single unit recordings were made from the buccal branch of the
anterior lateral line nerve. Both lateral line units and ampullar
units were encountered. These could be distinguished by the positions
of their receptive fields and the very low thresholds for electrical
stimulation of the ampullar units. Both types of units were
mechanically sensitive; only the ampullar units were electroreceptive.
These neurons were spontaneously active, and could be stimulated by
an electric field oriented such that the negative pole was at the
opening of the ampulla, while the opposite orientation had an inhib
itory effect.
The origin of electroreception in holocephalans and other
primitive fishes, and possible reasons for the loss of this sense in
more advanced fishes is considered. It is theorized that electro
reception arose early in the evolution of vertebrates; that the
ciliary electroreceptors are primitive characters which indicate an
elasmobranchiomorph affinity of the groups which have them, and that
v
the microvillar electroreceptor evolved independently. This theorJ
suggests certain alterations in the present phylogenetic relation
ships of primitive fishes, by the elasmobranchs,
placiP~ placoder~s,
holocephalans, certain chondrosteans and sarcopterygians in a
common line of descent. The possibility of electroreception in
other fishes, and extinct is discussed.
liviP~
Vi
CONTENTS
I. I~TRODUCTION --------------------------------------------- 1
II. LITERATURE REVIEW AND BACKGROUND INFORM.\TION ------------- 4
Holocephali ----------------------------------------- 5
Electroreception ------------------------------------ 18
Ampullae of Lorenzini: Literature Review------------ 24
III. ANATOMY OF THE AMPllLLAR AND LATERAL LINE SYSTEMS--------- 44
Introduction ---------------------------------------- 46
Methods --------------------------------------------- 47
Anatomy of the Lateral Line System ------------------ 51
Anatomy of the Ampullar System ---------------------- 67
Anatomy of the Cranial and Lateral Line Nerves ------ 103
Summary of Anatomical Studies ----------------------- 123
IV. BEHAVIORAL STUDIES OF ELECTRORECEPTION -------------------
Introduction ----------------------------~----------- :25
Methods --------------------------------------------- 126
Results --------------------------------------------- 129
Discussion ------------------------------------------ 135
(Continued)
vii
CONTENTS
(Continued)
V. NEUROPHYSIOLCGICAL STL'DIES OF ELECTRORECEPTION ----------- 138
Introduction ---------------------------------------- 138
Methods --------------------------------------------- 139
Results--------------------------------------------- 142
Discussion ------------------------------------------ 145
VI. OVERALL DISCUSSION--------------------------------------- 150
Phylogenetic Significance --------------------------- 150
Conclusions ----------------------------------------- 164
VII. FIGURES -------------------------------------------------- 171
VIII. REFERENCES ----------------------------------------------- 285
viii
INTRODUCTION
An animal's struggle for survival is dependent on its constant
interaction with the environment, so that the way in which it
perceives its world will profoundly affect many of its
biology. There is an increasing awareness that other animals
are not necessarily limited to the five main senses apparent to
humans, and thus may perceive a very different world.
Recent research has shown that some fish, notably many elasmo
branchs, have highly developed sensory systems which are extremely
sensitive to electric stimuli (Fessard 1974). This thesis
presents evidence that the second major line of cartilaginous fishes,
the Holocephali, also have electroreceptors, which appear to be
homologous to the ampullae of Lorenzini of elasmobranchs. The
hypothesis that the Holocephali might be electroreceptive seems
tenable on the basis of the taxonomic affinity of the elasmobranchs
and holocephalans, and certain similarities in the anatomy and
ecology of the two subclasses. However, there are substantial
differences between the two groups in regard to their anatomy
and behavior which would challenge the validity of this a priori
line of reasoning. Furthermore, the phylogenetic relationship
l
between the Elasmobranchii and Holocephali is controversial at
present (Zangerl 1973) .
Holocephalans appear early in the fossil record, approximately
400 million years ago, already distinct from the primitive elasmo
branchs of the time (Schaeffer and Williams 1977) . There is no
known intermediate fossil linking the Holocephali with the Elasmo
branchii, or any other group of fishes (May-Thomas and Miles 1971).
It is hoped that this study may be helpful in regard to some of these
phylogenetic
~uestions.
In addition, chimaeras are in many ways, and many aspects
uni~ue
of their biology have not been studied. Perhaps through studying
this sensory modality, certain of functional morphology,
~uestions
ecological relationships, behavioral aspects, and other processes
which have not been studied directly will be illuminated in these
fish. And conversely, owing to the features and habitat
uni~ue
of chimaeras, our concept of electroreception and its biological
significance may be expanded.
To prove that a fish is electroreceptive, it is necessary to
show that some behavior of the animal depends on the perception of
weak electric fields. Anatomical studies may then contribute by
providing comparative and functional anatomical evidence indicating
certain organs as putative electroreceptors. Neurophysiological
recordings from these organs in response to an applied electrical
stimulus is then necessary to prove that they are indeed capable of
responding to electric fields of the and intensity used
~uality
2
in the behavioral experiments. These three methods, behavioral,
anatomical and physiological, were used in this research.
This thesis is organized into six sections. A summary of the
taxonomy and phylogeny of the Holocephali is included in Chapter II
to provide necessary information for a discussion, in
backgro~~d
chapter VI, of the possible phylogenetic significance of electro
reception in primitive fishes. Also included in this background
section is a review of electroreception, the origin of
includiP~
electric fields in the environment, the structure of electroreceptors,
and a review of the literature concerning the ampullae of Lorenzini.
Anatomical studies of the apparent electroreceptive organs (the
ampullar organs), are presented in Chapter III, as well as a description
of the lateral line system, and the cranial and lateral line nerves.
Experimental evidence for electroreception in Hydrolagus colliei
is introduced in Chapter IV, ''Behavioral Studies of Electroreception,"
and Chapter V, "Neurophysiological Studies of Electroreception."
3