Solitary chemosensory cells: why do primary aquatic vertebrates

REVIEWS
Solitarychemosensorycells:
why do primaryaquaticvertebrates
need anothertaste system?
Kurt Kotrschal
A
generally more evenly distributed
The taste-like system of solitary
t the body surface of fish,
over the body surface20Jl. Howchemosensory cells (SCCs) has almost
a few chemosensory sysever, higher densities of SCCsmay
eluded scientific attention. This is
tems extract information
particularly remarkable, since recent
be found along the head than
&from a plethora of disalong body and tail, and SCCs may
surveys have revealed that this system
solved chemical#. Most fish have
of epidermal cells is widespread and
cluster around free neuromastsl4.
a keen sense of smell and, in addiabundant among the anamniotic aquatic
tion, they may carry abundant
Where are SCCs found and
vertebrates. In the rocklings (Gadidae,
taste buds on barbels or at other
Teleostei), high densities of SCCs occur
how abundant are they?
body surface#.
Consequently,
SCCsor oligovillous cells have
at a specialized dorsal fin. Recent
catfish have even been compared
evidence from this model indicates that
been found in the epidermis of
with tetrapod tonguess. However,
SCCs are narrowly tuned to dilutions
most primary aquatic vertebrates
fish also possess other skin theme
of fish body mucus and bile. Thus,
investigated2J. They are present in
receptors, resulting in an ill-charSCCs may sample the ambient water
most species of fish, including lamacterized ‘general chemosense’6J.
for the upstream presence of potential
preys, paleonisciform and teleost
The solitary chemosensory
actinopterygians, sarcopterygians
cells (SCCs) are the least known of competitors or predators. However, in sea
robins (Triglldae, Teleostei), SCCs seem
and even elasmobranchs (a ray,
these chemoreceptor&*. Staining
to be involved in finding food. Information
Raju clauat&‘). SCCshave not been
with methylene blue demonstrated
the presence of spindle-shaped
from many more species is needed to
found in a few species of fish, such
cells within the epidermis of some
explain why SCCs and taste buds have
as the benthic and sluggish northbeen maintained in parallel for such a
ern Atlantic Agonus cataphractus23.
teleost fishg. Because of their ap
parent basal contacts with nerve
long evolutionary period of time - from
The lack of a recurrent facial nerve
fibers and their ultrastructural
the age of the agnathans to that of the
(which innervates the trunk skin
resemblance to taste-bud cell+12,
most advanced teleost fishes.
in most fish) does not necessarily
these secondary sensory cells were
mean that SCCs are absent. For
assumed to be chemosensory; this
example, SCC-likecells innervated
Kurt Kotrschal is at the Konrad Lorenz
hypothesis was supported by elecby spinal nerves are present in the
Forschungsstelle and Dept of Zoology, University of
trophysiological recordings13J4.
finger-like free pectoral-fin rays of
Vienna, A-4645 Grtinau 11, Austria.
Throughout this review, ‘smell’
sea robins (Triglidae, Teleostei)llJ4.
refers to inputs provided by the
Among the amphibians, SCClike cells have been found only in
nasal olfactory mucosa, whereas
‘taste’ means inputs via taste buds. No proper term as yet
ranid tadpoleGJ5. However, it is uncertain how much this
limited phylogenetic distribution reflects the difficulties in
exists to name the SCC input and, to avoid confusion, none
is suggested.
searching for these cells in animals where the epidermis is
covered by a keratineous slough. A systematic re-investigation that includes cecilian and urodelan larvae may clarify
Structure of SCCs versus taste buds
the situation.
In most species, SCCs show a single microvillous apex,
Quantitative estimates of SCC densities over the body
which is sometimes furcated or even brush-like, and contacts
the ambient waters. In lampreys, similar cells carry a few surface are only available for 13 mainly ostariophysan teleapical microvilli, and are thus known as ‘oligovillouscells’l5-17. osts20Jl. These range from 200 SCCsmm-2 in the neon tetra
The obvious difference between taste-bud cells and SCCs (Hypessobrycon innesi) to 3000mm-2 in the roach (Rutilus
rutilus;Fig. la), with peak values of 21000 mm-2 in halos of
is that the former are part of a distinct organ, whereas the
100 km radius around free neuromasts. Thus, an averagelatter are embedded between unspecialized epidermal cells.
sized roach of 200mm body length may carry approxiEven when SCCsoccur at high densities (e.g. in the epidermis
mately 5 million SCCs. In eight species of cyprinids, 5748%
of the rockling anterior dorsal finIs) thin glial-likesheets from
epidermal cells prevent direct contact of adjacent SCCs.
of all epidermal chemoreceptors identified were SCCs, and
the remaining chemoreceptors were organized in taste
Taste-bud cells are innervated by intragemmal fibers,
and, similarly, SCCs form synaptic contacts at their bases
bud.9. A considerably higher density of approximately
with one to three (facial) nerve fiberG. SCCs are not inner1OOOOOSCCs
mm-2was found in the epidermis of the specialvated by perigemmal fibers, which may transmit tactile infor- ized anterior dorsal fin of rocklings (Fig. lb; see below)zJ6.
mation in taste buds, but the free spinal nerve endings that
are never far from any SCCmay be their functional analoglg. Cell-line orlgln of epidermal chemoreceptors
The fine structural similarity of oligovillous cells and
In many ostariophysan fishes (e.g. cyprinids and catfishy,
SCCSsuggests that they are part of a homologous (phyloexternal taste buds may cover the entire body surface and
genetically continuous) vertebrate cell line*.Their apex seems
aggregate at areas that frequently contact and locate food,
to reflect some phylogenetic change from oligovillous in the
such as lips, barbels4 or elongated fins. By contrast, SCCsare
110
o 1996, Elsevier
Science Ltd
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REVIEWS
agnathans to univillous in the gnathostomes, with a further
shift from a furcated tip of the villus to an unbranched tip
towards the perciformsQ.
The fine structural resemblance of SCCs to taste-bud
cells adds to the speculation that taste buds developed during the early phylogeny of (agnathan) vertebrates by accumulation of SCCs(Refs 2,8,11).This direction of evolutionary
change is plausible, because it would be from the simple
(SCC)to the more complex structure (taste bud). However,
the opposite direction of evolutionary change (which would
imply that SCCs are disaggregated taste buds) cannot be
rejected, because there are no extant taxa with either SCCs
or taste buds. Lampreys have taste-bud-like structures, the
so-called terminal budsl6, in addition to their oligovillous
cells. As a third possibility, SCCs and taste buds may have
developed independently.
The question of cell-line relationships of SCCsand tastebud cells may be of minor importance, since increasing evidence indicates that these secondary epidermal chemosensory cells do not originate from neural crest material, but
are induced from undifferentiated epidermal stem cells27J8
by the innervating nerves. Thus, the ability to differentiate
into epidermal chemoreceptors would mainly be due to a
stimulating potential of the innervating (facial or even spinal) nerves. This, of course, does not explain why some of
these nerves induce and innervate SCCs and others induce
and innervate taste buds. It is not even known whether SCCs
and taste buds are always innervated by different nerve
fibers, or whether a single (facial) fiber may sample both
structures.
SCC function: the rockling anterior dorsal fin
Because of the difficulties of studying SCCsin generalized
distributed systems2J1, most of our present knowledge on
SCCs is from studies of the anterior dorsal fin of a few species of rocklings (Gadidae, Teleostei). This fin is a complex
chemosensory organ, with approximately 100000SCCsmm-2
(approximately 5 million SCCs in tota1)[email protected] structure of
cells, their innervation and synapses, representation in the
central nervous system (CNS), sampling movements of the
fin and, to some extent, the function and biological roles of
SCCshave been investigated in this model. From these studies, inferences have been made about the function of distributed SCCsystems21.
It has been demonstrated that several hundred SCCsconverge onto a single facial nerve fiber along the anterior dorsal
fin of rocklingsl2,17,19,26.29.
These fibers are somatotopically
represented in a distinct dorsal part of the brain-stem facial
lobe26.However, the higher-order brain connections are not
particularly distinct from the taste-bud system, and the primary somatotopy is not preserved in ascending or descending connections21 (K. Kotrschal and T. Finger, unpublished
data). For these reasons, it seems adequate to consider SCCs
as a taste (facilis) sub-system.
Chemoresponses could only be recorded electrophysie
logically from the moving fin. Furthermore, responses were
only elicited by a narrow spectrum of stimulil4JOJ1,including dilutions of heterospecific fish body mucus, fish bile or
human sputum, but not by typical taste stimuli, such as food
extracts and amino acids. The fin samples by an undulation
of lo-20 Hz, depending on the temperature. Specific stimulation caused a decrease in opercular breathing movements,
which is associated with alertness, and an increase in sampling frequency of the fin32J3.Therefore, it was concluded
that the rockling anterior dorsal fin is a low-threshold bulkwater sampler, which probes for the upstream presence of
other fish, including potential predator&*l.
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(4
Taste
(b)
Fig. 1. (a) Solitary chemosensoty cell (SCC) system of a roach (Rutilus rutilus) as
an example of a generalized distributed system. Length of the fish is approximately
200 mm. The cross-section through the head skin (top) shows a taste bud and an
SCC. The epidermis is approximately 50 km thick, and 1 mm* epidermis may contain a few thousand SCCs. (b) A specialized aggregated SCC system in the rockling
(Gaidropsarus sp.) anterior dorsal fin. Length of the fish is approximately 200 mm.
Fin rays on top of the fish are approximately 3 mm in length and 0.1-0.2 mm in
diameter. The ray epidermis is approximately 30 pm thick, and 1 mm2 ray epidermis contains approximately 100000 SCCs.
These results render it unlikely that SCCs are the morphological substrate for the ‘common chemical sense’ (sensu
Parke@2JJl, which mediates high-threshold avoidance reactions to harmful chemical stimuli. This unspecialized them@
sense7JJ is likely to reside in free trigeminal (head) and spinal
(body) nerve endings34.
Sampling in SCCs and taste buds
Fluid flow decreases towards surfaces, resulting in relatively stagnant ‘boundary layers’. Stimulus molecules can
only access sensory surfaces by slow molecular diffusion
through these layers. Enhanced flow decreases the thickness of boundary layers and, therefore, accelerates the access of chemicals to receptor sites. This principle applies to
both taste buds and SCCs.
In the SCCsof the rockling anterior dorsal fin, responses
could only be recorded from the moving fin, where undulation frequency determines the access of the stimulus to
receptor surfaces. Therefore, the response intensity of the
system at constant ambient concentrations of stimulus depends upon both the physiological properties of the receptors and fluid flow14.This also means that individuals can
only extract information on stimulus strength by integration
of flow velocities. In rocklings, this may be achieved by an
integration of the motor activity of the fin with sensory gain
in the brain stem21.In other fish, aggregations of SCCsaround
free neuromasts can be observed20v21;
thus, an integration bc
tween neuromast and SCCinput may be achieved within the
brain. This is supported by l,l’-dioctadecyl-3,3,3’,3’-tetramethylindo-carbocyanine (di1) tracings of secondary facial
lobe connections within rockling brains (K. Kotrschal and
T. Finger, unpublished data).
By contrast to SCCs, flow may be generally of minor
importance for taste-bud function, because taste buds seem
to be most useful for the co-localization of tactile and chemical stimuli2 (i.e. allowing discrimination of palatable items
upon touch). However, flow may be important in cases such
as catfish barbels, where taste buds can provide orientation in chemical gradients 35.Also, in the taste-bud pore,
111
REVIEWS
V’
Pike
Fig. 2. Fish downstream of a potential predator (a pike, Esox lucius) exploring the
odor plume. Epibenthic fish samples the plume with the SCCs at its body surface
by swimming a zig-zag path. Benthic rockling samples the plume with its anterior
dorsal fin while at rest.
the supporting cells provide a peculiar thin-layered mucus
environment for the apical villous chemoreceptorsir. This is
not the case for SCC apices, which reside within the relatively thick body mucus.
By contrast to the rockling anterior dorsal fin, the distributed SCCsin other fish are not mounted on a specialized
support that can be moved independently of the body. However, it is reasonable to assume that currents are also indispensable for SCC sampling in generalized distributed systems. Such currents may be generated by the environment,
but are predominately produced by active swimming movement.+. Thus, swimming in fish is not only a means of locomotion; it also serves to actively sample the environment for
chemical (as well as visual and electrical) stimuli, analogous
to sniffing. Dashing and zig-zagging are part of the behavioral responses of some fish to the presence of alarm substance36J7,and such behavior was interpreted previously as
predator avoidance or distraction behavior. However, increased swimming activity with no clear spatial vector may
also serve to sample the environment for (chemical) stimuli
and to use chemosensory organs, including SCCs, to their
full potential. High-resolution swim-path analysis has indeed shown an increase in swimming velocity and unsteady
swimming in European minnows stimulated with potential
predator odor (dilutions of trout body mucus)38J9.
The evolutionary significance of SCCs
The rockling anterior dorsal fin provides the basis for
speculations on the evolutionary benefit of SCCsystems. The
dorsal fin confers a unique advantage on substrate-orientated night-active rocklings as compared with the distributed SCC systems of all other fish: rocklings may scan the
upstream water for the presence of fish, including potential
predators, without having to leave their sheltersss. Comparisons between successive measurements would allow a
rockling to judge the situation ahead of the fish and to adjust
its own behavior accordingly. Water currents generated by
the active sampling movements of the fin are necessary to
trigger responses from their SCCs(Fig. 2)iJ. To generate flow
at their body surfaces, all other fish would have to sample
odor plumes by swimming through them (Fig. 2). Although
these fish can collect quick and precise information on spatial structures and dynamics of odor plumes, active swimming potentially increases their exposure to predators.
112
Such SCCsystems may have evolved as bulk-water samplers, providing the fish with useful information on the presence of other fish upstream. Evidence in rocklings indicated
that heterospecific fish mucus triggered responsesl4, and
that proper stimulation of rocklings caused a cessation of
opercular breathing movements, which can be interpreted
as an arousal response (see above)3zJs. Therefore, it was assumed that a major ecological role of SCCs may be predator
avoidance. However, suction-electrode recordings in isolated fin rays showed that conspecific bile may also be a potent stimulus o<. Kotrschal and K. Doving, unpublished data).
In general, information on the upstream presence of other
fish may affect intra- and interspecific spacing, competition,
or even home range and habitat recognition.
If predator avoidance is a major function of SCCsystems,
it can be predicted that the system should be particularly
well developed in fish that are most susceptible to predation:
juveniles or species that remain relatively small. However,
no relationship between body size and SCC densities was
found in 12 species of teleosts*O.The ontogenetic develop
ment of SCC densities in zebrafish (Danio rerio) shows a
steep positively allometric increase of SCCdensities relative
to body surface during early postlarval growth, when small
juvenile fish are probably most susceptible to predation (K.
Kotrschal and A. Hansen, unpublished data). Clearly, these
data are still insufficient to judge a possible role of SCCs in
predator avoidance. Rather than body size, predation pressures (for example, in the original habitats of the species) are
probably relevant. SCC densities have been shown to increase in carp as a response to acidification40, but no other
data exist about possible adaptive changes of SCCdensities
in individuals.
A number of recent publications indicate a remarkable
complexity in chemical predator-prey communication and,
hence, stress the importance for potential prey fish to
keenly distinguish between different chemical stimuli from
conspecifics (alarm substance) and predators (Refs 41-43).
Experimentally anosmic fish do not behaviorally respond to
relevant stimuli, such as chemicals from predators44, but this
does not necessarily disprove an SCC involvement in this
kind of chemo-communication, because of the following
points: (1) Rendering fish anosmic dramatically decreases
their overall activity, which makes behavioral effects of
chemo-stimulation hard to detecPJ9. (2) Appropriate methods allow subtle behavioral changes in anosmic fish in
response to food stimuli to be detected, but responses to
body-mucus dilutions of potential predators were ambiguou.+‘J3,38,39.
(3) Both SCC and olfactory inputs may need to
be integrated within the brain to evoke motor outputs*l. This
may occur within the telencephalon, which is reached by
viscerosensory input via lemniscal pathways4s, and if this is
the case, only electrophysiological recording from the telencephalon, not behavioral experiments with anosmic fish,
will be conclusive.
What we ought to know: why one should be
extremely cautious in generalizing
As indicated in this article, the majority of functional
results on SCCsare from rocklings, which are only a few spe
ties out of more than 20000 teleost species. However, support for the present rockling-based generalization is
provided by the observation that oligovillous cells in lampreys responded vigorously to water in which frozen trout,
a major lamprey predator, had been allowed to thaw13.
Of all the aquatic vertebrates with SCCs (excluding rocklings), the source of innervation has only been established
in the sea robins, where SCC-likecellsll seem to be supplied
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REVIEWS
by spinal nerves46and respond to food-related stimuW. This
is almost in complete contrast to the results in rocklings,
and underlines the need to be extremely cautious when generalizing about SCCs with our present knowledge. The majority of other unexplored SCCsystems may either be facially
or spinally innervated and may even functionally differ from
those in both rocklings and sea robins.
Where we ought to go from here
Studies on the innervation and function of distributed
SCCsystems outside the rocklings are urgently needed. However, rocklings will remain one of the most important models
in SCCresearch, mainly because of the abundance of SCCsin
their anterior dorsal fin and because of the accessibility of
this system for research. Recordings from single facial nerve
fibers and patch-clamp recordings from isolated SCCs are
required. Furthermore, rockling SCCs should be used as as
a bioassay during further isolation and characterization of
the active stimulus components. Finally, CNSrecordings in
rocklings and other fish are needed to elucidate the potential
crosstalk between olfactory and SCCinputs.
Against such a background of morphological and functional data, further behavioral experiments will help to clarify
the ecological roles of SCC systems and to explain why the
primary aquatic vertebrates have kept their SCCs, in parallel
with taste buds, over such long evolutionary periods.
Acknowledgements
I thank the ‘Verein der Fijrderer’ and the
H.v.Cumberland-Stiftung
for permanent support.
I am particularly grateful to Mary Whitear, Jelle Atema,
Kjell Doving, Tom Finger and Rob Peters, my colleagues
and friends who have contributed significantly to our
present knowledge about SCCs.
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A molecularapproachto the evolutionof
vertebrate pairedappendages
Paolo Sordino and Denis Duboule
he origin and the strucOver the past few years, genes involved
a comparative analysis of molecutural transformation
of
in the ontogenesis of tetrapod limbs
lar mechanisms.
paired appendages is a
have been isolated and characterized.
The elusive origin of paired
fundamental trait of verteSome of the developmental mechanisms
appendicular systems has pre
brate evolution. Since the recogniresponsible for the morphogenesis
eluded the identification of the
tion of structural homology among
of these complex structures can now
progenitor organisms from which
tetrapod limbs, the existence of a
be investigated through a new
such endoskeletons originated.
unique developmental programme
approach. In addition, these genes can
Thus, the history of fins remains
for limb patterning has been proserve as tools to re-evaluate some
speculative. It is generally be
posed. Basic instructions would
aspects of the long-standing question
lieved that early chordates had a
constitute an informational groundof the Rn-to-limb transition. Comparative
continuous median fin fold along
plan on which species-specific
molecular developmental biology is
the dorsal-ventral axis. This fold,
neontological customizations are
similar to that found in cephaloproviding new insight into the
generated. Paleontological and
similarities and differences in the
chordates and some urochordate
embryological (experimental and
morphologies of these homologous
larvae, may have allowed unducomparative) observations have
latory movement in the aquatic
structures.
led to various conceptual frameenvironment. A further improveworks for understanding the origin
ment of hydrodynamism and moPaolo Sordino and Denis Duboule are at the Dept of
and evolution of tetrapod limbs
tility was achieved by the ap
Zoology and Animal Biology, University of Geneva,
(reviewed in Refs 1,2). Yet our
pearance of fin-like paired lateral
Sciences Ill, Quai Ernest Ansermet 30,
knowledge of the transformational
structures during the evolution
1211 Geneva 4, Switzerland.
sequence between lower and
of early vertebrates. The jawless
higher vertebrates is still too
ostracoderms (Ordovician and
scarce for the evolutionary history
Devonian; 480-350 million years
of lateral appendages to be described unequivocally. In ago) exhibited different types of appendages. Spines, cornuae and plates1 were probably derived from the dermal
this context, the study of the evolution of basic morphobody armour, and conferred stability rather than propulsion,
genetic and molecular programmes in vertebrates may be
in the absence of air-filled swim bladders. However, some
informative. That the underlying biomolecular systems
have retained some important features during millions of fossil ostracoderms show anterior paired appendages,
years suggests that minimal variations within such sys- which may be representative of the oldest genuine pectoral
tems may have been a source of morphological evolution
fins. Nevertheless, the earliest occurrence of both flexible
(macroevolution)sv4. To learn how conserved molecules
pectoral and pelvic fins (phylogenetically related to modern
may generate morphological diversity requires detailed
fish fins) has been found in a heterogeneous array of early
functional comparisons, with emphasis on an evolutionjawed fish fossils from the late Silurian (410 million years
ago)iJ. It is clear that this innovation was a successful soluary perspective. Here, we use recent molecular data
(obtained while studying teleost fin morphogenesis) to
tion to the need for locomotion, since these systems have
assess how evolutionary scenarios built upon palaeonundergone wide functional radiation and morphological
tological and ontogenetic evidence can be reconciled with
evolution during vertebrate phylogeny.
T
114
0
1996, Elsevier Science Ltd
TREE vol. II,
no. 3 March
1996