Chapter 19
Integumentary Sensory Organs in
Crocodilians
Sarah Gabriel
Portland State University 2013
Sarah Gabriel
19.1 Introduction
Crocodilians, which include alligators and
crocodiles, have a tough exterior with
scales covering their dorsal and ventral
surfaces. Living on earth before the dinosaurs, these reptilians have evolved a
structure that has helped them adapt to the
changing environment of earth. This structure is called an integumentary sensory organ (ISO). Integumentary is a term, which
refers to the skin surface of organisms. In
the case of crocodilians their skin possess
many tiny ISOs that look like tiny protuberances on the crocodilian scales. The
ISOs location on their skin allows them to
gather information on their environment.
The ISO distribution across crocodilians
vary in location, but are similar in morphology and function.
Historically, these tiny sense organs of
crocodilians have been observed by earlier
researchers but were not well understood
and mainly just observed and suggested
as a possible tactile sensitivity organ. Yet,
they are now known to serve as a sensory
organ, which includes tactile sensitivity.
ISOs as a sensory organ can function for
water disturbance detection (track prey or
avoid predator), mating, reproduction, and
osmo-regulation.
ISOs have been referred to as many
different terms in the past depending on
the research being done and the findings
from that research. Water surface dis-
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CHAPTER 19. INTEGUMENTARY SENSORY ORGANS IN CROCODILIANS
Figure 19.1: Distribution of integumentary sensory organs in extant crocodilians based on phylogeny.[1]
ruption receptors and dome pressure receptors have been used as terms to name
these organs while also functionally describing it. Since the sensory skin organ
has been found to serve many different
sensory functions in crocodilians, the term
integumentary sense organ is the most inclusive term for describing this organ and
will be referred to as such.[1]
19.2 Location
Integumentary sensory organ distribution
in crocodilians varies based on species
phylogeny, as seen in figure 1.1. In Alligatoridae (American alligator and caimen)
ISOs can be found distributed in the cranial region around the mandibular and
maxillary region of the mouth, while in
Crocodilidae (true crocodiles and gravials)
ISOs can be seen as in the cranial region
as well as their post-cranial region of the
rest of their body. [1]
In terms of ISO density, in alligators
the greatest ISO density is found around
their teeth region as well as their dorsal
maxilla region, in crocodiles the is also a
high density in the cranial region yet less
than that of alligators. [1] In crocodylids,
since their ISOs are also seen to be dispersed onto the rest of their body besides
the head, it has been observed that ISO
density in the rest of their integumentary
regions (post-cranial region) show that
ISOs are less dense in concentration, but
appear to be located as one or more ISOs
per scale. [1]
It is currently not well known why ISOs
are distributed differently in the Crocodilidae and Alligatoridae since speciesspecies research comparison on ISO distribution has not been currently conducted
and divergence analysis between the two
in association with ISO distribution has
yet to be done. What is certain is that both
species share the commonality of ISO distribution in the cranial region.
19.3 Structure of ISOs
The integumentary sensory organ receptors in both alligatorids and crocodylids
follow the basic structure as seen in figure 1.2.[1]They appear as dome shaped
structures. The whole structure is com-
19.4. NERVE INNERVATION
posed of many nerves and tissues to make
up a whole ISO. There is a keratin layer
on the most superficial surface at the stratum corneum layer at the epidermis, with
nerve fibers , such as free nerves which
are afferent nerve endings that have unspecialized capabilities, but are through the
epidermis. Also, coming from the dermis
towards the epidermis layer are discoid
(flat shape) receptors.
The deepest layer contains many nerve
fibers, as well as a dermal merkel complex.
The dermal merkel complex is a dermal
(skin) receptor that deals with an animal’s
sense of touch and object discrimination
(texture). This complex acts in conjunction with afferent neurons that branch off
as nerves, which can be covered in a perineural sheath (insulation of sensory nerve
fibers). In the dermal layer there are encapsulated and unencapsulated lamellated
corpuscles. Lamellated corpuscles serve
as mechanoreceptors that allows for sensitivity to vibration and pressure. Also,
according to figure 1.2, the melanocytes
(melanin producing cells) are ubiquitously
placed beneath receptors; giving ISOs
their dark pigmentation.
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Figure 19.2: Schematic diagram based on samples from A.
mississippiens is and C. niloticus cranial and body receptors.
Cap, capillary; Discoid, discoid receptor; En LamC, encapsulated lamellated corpuscle; FBR, free branched receptor of
the connective tissue; Ker, keratin Ker, keratinocyte; LamC,
lamellated corpuscle; Mel, melanocyte; PNS, perineural
sheath; RAx, branched receptor axons of the ISO connective
tissue; StC, stratum corneum; StL, stratum lucidum; StS,
stratum spinosum.[1]
19.4 Nerve Innervation
In the cranial region of both alligatorids
and crocodylids there is the trigeminal
ganglion that gives off three nerves, the
ophthalmic nerve, maxillary nerve, and
the mandibular nerve. The ISOs of the
cranial region for instance are constantly
innervated when initiated by a stimulus, of
which has been tested and observed extensively in the trigeminal ganglion afferent
cell bodies of the cranial region. Most of
the receptive fields are located in the jaw
region across the mandible and up towards
the maxilla. Some of the largest receptive
fields in the alligatorids and crocodylids
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CHAPTER 19. INTEGUMENTARY SENSORY ORGANS IN CROCODILIANS
are located within the mouth region (teeth,
tongue, and upper palate). According to
figure 1.3a it can be seen that in the cranial region, the mandible and maxilla have
their own designated nerves, which give
off to a diverse branching pattern of fibers
for nerve innervations in those regions. [1]
Figure 19.3: Innervation of the cranial ISOs by the trigem-
inal nerve. (A) Side view of the rami of the trigeminal nerve
with hypertrophied mandibular and maxillaryand maxillary
branches comprising a network of finer fibers innervating
regions where ISOs are present. Branching patterns were
drawn from Sudan Black B preparations (see Materials and
methods). The brain is shown to indicate the relative location
of the trigeminal ganglion. Cb, cerebellum; gV, trigeminal
ganglion; OB,olfactory bulb; OT, optic tectum; Sp, spinal
cord; Tel, telencephalon. Scale bar, 1cm. (B) Example photograph of Sudan Black B preparation showing the darkly
stained processes of the maxillary nerve within the cleared
whole-mounted specimen. Scale bar, 750m. (C) Transverse
section of a mandibular nerve from C. niloticus. More than
46,000 myelinated axonsmyelinated axons (s.d. =2700), as
seen in the inset, were present within the nerve whereas
fewer (3600200) were present in the ophthalmic component.
Scale bar, 50m.[1]
19.5. FUNCTION OF ISOS
19.5
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Function of ISOs
With the ISOs location in important cranial and post cranial regions (crocodylids)
as well as ISO connection to important
nerves such as the trigeminal nerve that
gives rise to three other nerves of the
opthalamic, mandibular, and maxillary region, it is obvious that ISOs have great importance. The ISOs prime locations allow
for tactile sensitivity as a mechanoreceptor for various functions, which have been
Figure 19.4:
shown to include:
• Water Disturbance Detector
• Mating and Reproduction
• Osmo-regulation
As a mechanosensory organ, ISOs in
crocodilians have been seen to function
as a water detection organ, allowing for
the detection of water disturbances in the
environment. Alligators have the ability
to orient themselves to water disturbances.
This has been demonstrated by covering
the head region of an alligator with a plastic elastomer. When the head region of the
alligator was covered, the alligators ability
to detect water disturbances and to orient
them to the disturbance was gone. [2]
Body regions bearing ISOs are employed
during courtship and reproduction: (A) two female Cuban
crocodiles, Crocodylusrhombifer, engage in rubbing their
ISO-bearing jaw regions on each other and the male (left),
as a prelude to copulation with the male; (B) ISOs are well
developed in hatchling crocodilians. Circles indicate ISOs
on a hatchling West African dwarf crocodile, O. tetraspis,
emerging from its egg. [3]
These physical orientation behaviors in
alligators can include either a head turn or
a full body turn, but can vary according
to location and if any obstructions are in
the way. The orientation behavior is seen
to only occur when alligators have their
faces within the air-water interface. Yet,
when they have their head submerged or
completely submerged underwater, their
water detection ability drops, and they rely
on other detection capabilities. [2]
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CHAPTER 19. INTEGUMENTARY SENSORY ORGANS IN CROCODILIANS
It has been found that the ISO can
also serve in the mating and reproductive behaviors of crocodilians. Also, observational research on the behavior of
crocodilians shows them using their ISOs
specifically during courtship. As seen
on figure 1.4A, tactile stimulation of the
ISOs can be seen in crocodylids during
courtship. This rubbing of the ISOs between crocodylids is proposed to be a precopulatory behavior, which can occur between females and females and males and
females.
Crocodylids exhibiting reproductive behavior have been seen to use their ISOs as
an aid in nest site locating; which is only
seen in crocodilian females. The females
can utilize their cranial snout, which is
covered in a high concentration of ISOs
when digging holes and testing the substrate temperature for potential egg laying sites. The ISO being used in nest site
tracking by a female crocodylids has been
linked to temperature dependent sex determination in certain species of crocodylids;
the varying substrate temperature sense by
a female crocylids ISOs can determine the
sex of their offspring. [3]
There have been numerous studies done
to test if crocodilians utilize their ISOs
Figure 19.5: ISO flattens in response to exposure to a
hyper-osmotic sea water solution (full-strength sea). [4]
to determine water salinity, thus functioning as osmoreceptors. Two studies noted
have produced contradictory claims regarding crocodilians ability to use ISOs
are osmoreceptors. One study concluded
that the integumentary sensory organ itself
would mechanically flatten upon being exposed to a hyper-osmotic solution, such
as salt water (figure 1.5). [4]
This ability allows for osmo-regulation
of crocodylids, so that in hypo-osmotic
water it will sense that the water environment is hypo-osmotic to its own body and
will drink the water opportunistically for
hydration, verses when it is in a hyperosmotic water environment it will avoid
drinking too much of the water. Yet, this
study was done on Crocodylus porous, a
known estuarian crocodile. Since this was
an estuarian crocodile, it is important for
its body to sense the osmolarity of its environment through its ISOs. [4]
19.6. CONCLUSIONS
In contrast to the work on Crocodylus
porous, studies done on the Nile crocodile
show no response to osmotic changes in
the environment. In the latter study, there
was no afferent nerve responses detected
from the post-cranial ISOs upon exposure
to a hyperosmotic solution, thus they do
not function as osmoreceptors. It is also
seen that in alligatorid have no afferent
nerve responses upon exposure to a hyperosmotic solution also well. [1] Possibly further research into other species of
crocodilians would allow for more definitive evidence on ISOs role as an osmoreceptor.
19.6
Conclusions
The integumentary sensory organs of
crocodilians are now considered after
years of speculative research to be sensory organs. These sensory organs are differentially distributed in crocodylids and
alligatorids, yet have similar functions in
prey detection (water disturbances), mating/reproduction, and osmo-regulation.
Further research on crocodylids shows
that ISOs also function in mating and reproduction, which is important in an environment with many chemical cues that
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need to be distinguished and mating is vital for fitness.
As for osmo-regulation, it is currently
debatable whether or not ISOs can function as osmoreceptors since there are contradicting findings. Possible future research could be done on ISOs across
crocodilian species which live in different
environments, such as freshwater verses
salt water living crocodilians. Osmoregulation between different species most
definitely can be possible and should be
taken into account in research conclusions
across different species.
Besides ISOs being seen in crocodilians,
ISOs could have existed in pre-historic extinct crocodilians as seen in fossil findings. It is speculated that ISOs could
have been around since prehistoric times.
Cranial fossils of semi-aquatic crocodilians show foramina where ISO nerves
would have gone through. Foramina are
holes in the fossilized skull where cranial nerves, arteries etc would have passed
through. Strictly, terrestrial crocodilians
do not have such foramina. [2]
Current day crocodilians that live semiaquatically have such foramina, thus ISOs
could have evolved early in Jurassic
times. It has been noted that special-
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CHAPTER 19. INTEGUMENTARY SENSORY ORGANS IN CROCODILIANS
ized cutaneous organs (skin related organ)
with sensitivity such as ISOs are present
in lizard families of Inguania, Gekkota,
Scinocamorphs and Anguimorpha, yet
their skulls lack the foramina (holes in
fossilized skulls where cranial nerves etc
passed) seen in extant crocodilians. [2]
Overall, sensory organs specialized for
tactile sensitivity etc have evolved in reptilians, which shows that it serves a evolutionary advantage especially in the dangerous ever changing freshwater and ocean
environments.
Bibliography
[1] Leitch, Duncan, Catania K., Structure,
Innervation and Response Properties
of Integumentary Sensory Organs in
Crocodilians..Journal of experimental
biology, 2012, p. 4217-4230
[2] Soares D., Neurology: An Ancient
Sensory Organ in Crocodilians.. Nature 417.6886, 2002, p. 241-242
[3] Peter, Watanabe M., Crocodilian Behavior: A Window to Dinosaur Behavior?.Historical Biology 23.1, 2011, p.
73-90
[4] Jackson K., Brooks D., Do Crocodiles
Co-opt Their Sense of ”touch” to
”taste”? A Possible New Type of Vertebrate Sensory Organ.. AmphibiaReptilia 28.2, 2007, p. 277-285
[5] von During M., The Ultrastructure of
the Cutaneous Receptors In the Skin
of Caiman crocodilus.. Abhandlugen
Rhein. Westfa. Akad 53, 1974, p. 123134
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