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the Tricas Lab | ![]() |
Tanner Choudrhy (parrotfish foraging behavior)
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Tanner Choudhry (MS) |
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I will be studying the foraging behavior of parrotfishes on coral reefs of Hawai'i. |
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Christine Ambrosino(MS Zoology 2012)
Differential behavior of ampullary subunits in the electrosensory system dof the scalloped hammerhead shark (Sphyra lewini)
Abstract: The electrosensory system of elasmobranchs consists of discrete networks of gel-filled canals that connect to a specific subgroup of a subcutaneous structure called an ampulla. This project tested the functional subgroup hypothesis that predicts functional differences among the ampullary subgroups using the scalloped hammerhead shark, Sphyrna lewini. To examine electroorientation behavior, the reaction of sharks to electrical dipoles was digitally recorded on video. After control trials, sharks then had certain ampullary pore fields blocked with non-conductive petroleum jelly and again exposed to the same dipoles to observe potential changes in orientation behavior. The entire cephalofoil and either the right or left half of the cephalofoil were blocked in trials to determine the efficacy of the treatment protocol. The Buccal (BUC) and Superficial Ophthalmic anterior (SOa) ampullary pores were then inactivated. The BUC and SOa pore fields were chosen for study due to their location on the cephalofoil and pore number. The majority of sharks oriented to the dipole less than 12cm away and at an angle of less than 40 degrees from the dipole axis. Sharks with blocked BUC pores demonstrated fewer orientations to the simulated prey field (p = 0.008), although they still fed and swam normally. The manipulated sharks also showed decrease spiral behavior in relation to the other orientation types, and increased their overshoot behavior with blocked SOa pores. Thus, the functional subunit hypothesis is supported by this study and the entire ampullary pore field was demonstrated to be necessary for proper orientation within a dipole field.
James L. Bradley IV (MS Biology 1996)
Prey energy content and selection, habitat use and daily ration of the
Atlantic stingray, Dasyatis sabina
Abstract: Batoid elasmobranchs are important demersal
carnivores in most marine ecosystems, but their trophic dynamics are largely
unknown. The Atlantic stingray, Dasyatis sabina, is a common demersal
carnivore on small invertebrate prey in the Indian River Lagoon system. This
study assessed the energy content and digestive processing of natural prey of D.
sabina and its foraging behavior in the field. Caloric density (cal/mg AFDW)
did not differ across prey groups of amphipods, isopods, ophiuroids, mysids,
polychaetes, and bivalves. The highest caloric content per individual item was
in the polychaete Arenicola cristata (150 cal/ind), and the bivalves Brachidontes
exustus (153 cal/ind) and Amygdalum papyrium (60 cal/ind). Ophiuroid
disks, which are an important summer prey, had higher caloric content in August
(63 cal/ind) than in April (29 cal/ind) or December (22 cal/ind). Isopods,
mysids, and the three species of small polychaete had lower caloric contents of
10-20 cal/ind. Amphipods, the most frequent prey, and the polychaete worm Cistenides
gouldii had the lowest caloric content at 1-5 cal/ind. Amphipods were the
most abundant prey type in the habitat in June 1995 and occurred in stingray
stomachs more frequently than expected for random foraging. Stingray feeding
activity was most common in the sand and sand-seagrass interface subhabitats but
uncommon directly in seagrass. The low frequency of ophiuroids, mysids,
polychaetes, and bivalves in the diet may be due to their low abundance. Three
feeding strategies are proposed to explain the dietary habits of D. sabina:
1) numerical maximization of small, abundant, low-energy prey such as amphipods
and isopods which have a negligible or low handling time, 2) caloric
maximization of prey that are low in abundance or fluctuate seasonally such as
polychaetes, and 3) the seasonal caloric maximization strategy, a subset of
strategy two, in which energy content from ophiuroids is maximized over time.
Digestive index of prey and variation in the stomach fullness ratio indicate
that D. sabina fed continuously throughout the diel cycle. Daily ration
in July was estimated at 2.52 %BW/d or annually at 9.2 x BW/yr and indicates
that D. sabina could consume 15,150 amphipods/day or about 48 kcal/d.
Daily ration in summer months is similar to that reported for large piscivorous
sharks (0.6 - 3.2 %BW/d), and benthic feeding teleosts (1.3 - 3.3 %BW/d). The
annual ration of rays rivals that of the warm-bodied mako shark (11.6 x BW/yr).
Michael
Callahan (BA Biology 1997)
Summary: I studied the distribution of cutaneous receptors in the
Atlantic stingray Dasyatis sabina. We used silver stain techniques to
identify individual neurons and their innervation patterns at different regions
of the body.
David A. Cook (MS Biology 1994)
Temporal patterns of food habits of the Atlantic stingray, Dasyatis sabina
(Lesueur, 1824) from the Banana River Lagoon, Florida
Abstract: The Atlantic stingray, Dasyatis sabina, is one of the most abundant large fishes in the Indian River Lagoon system, but little quantitative information exists on its diet. Stomach contents of 320 rays were examined over a 20-mo period to determine prey types, seasonal shifts in prey selection, and differences in diet between sexes. Stingrays were sampled from a shallow sand-bottom, seagrass habitat of Halodule wrightii in the Banana River, Florida. The diet consisted of more than 27 different prey types at the family level. Small crustaceans, polychaetes and echinoderms were the major prey. Amphipod and isopod crustaceans were the most important prey items by the Index of Relative Importance in the total diet of both sexes. Amphipod and ophiuroid prey exhibited annual importance in the diet. Male and female diets did not differ in dietary composition. Prey diversity among stomachs was highest in fall and winter months and lowest in summer when amphipods were the major prey. It is concluded that Dasyatis sabina is an opportunistic benthic predatory that exhibits temporally predictable dietary shifts among amphipod and ophiuroid prey.
The distribution and density of GnRH-RIII receptors in sensory processing regions of the brain of the monogamous multiband butterflyfish, Chaetodon multicinctus
Gonadotropin-releasing hormone is a neuropeptide that affects reproductive behavior in vertebrates. The multiband butterflyfish, Chaetodon multicinctus, is a monogamous, territorial model for social behavior and neuropeptide interactions. Previous studies determined the location of GnRH-secretory neurons in Chaetodon multicinctus, but receptor locations, which show sites of action, remain unknown. The goal of this study was to use immunohistochemical techniques to examine whether changes in distribution or density of GnRH receptor III cells could be related to changes in reproductive behavior. GnRH-RIII cells are located in sensory and motor processing regions throughout the brain. Numbers of GnRH-RIII cells per nucleus were compared across sex and reproductive season, and there was a difference in the tectum, glomerular nucleus, nucleus isthmi, cerebellum, and preoptic area. While there is no difference in the number of GnRH-secretory cells across reproductive season, the difference in receptor number may change the magnitude of its effect.
Paul
M. Forlano (MS Biology 1997)
Differential distribution of gonadotropin-releasing hormone variants in the
elasmobranch brain: function and evolution
Abstract: Gonadotropin-releasing hormone (GnRH) is a
decapeptide hormone that is best known as a reproductive regulator in
vertebrates for its control over the release of gonadotropins from the
pituitary. The basic structure of this molecule includes at least nine different
forms across the vertebrates. Some of these forms are believed to serve
extrapituitary functions, as indicated by their wide distribution throughout the
brain. While chicken II GnRH (cII) is considered the most evolutionarily
conserved variant because it is found to coexist with one other form in all the
jawed vertebrate classes, dogfish GnRH (df) is found exclusively in elasmobranch
fishes. Although the df and cII GnRH forms were previously isolated and
sequenced in the elasmobranch, their regional distributions and specific
functions in the brain are unknown. Studies on bony fish, amphibians, reptiles,
birds and mammal show cII GnRH to predominate in the midbrain, whereas a taxon-specific
form is concentrated in the forebrain, including endocrine areas of the
hypothalamus. This study examines the distribution of df and cII GnRH-immunoreactive
(ir) cell bodies and fibers in the brain of the Atlantic stingray, Dasyatis
sabina, by immunocytochemistry with specific antisera raised against these
variants and preabsorption of the antisera with homologous and heterologous
peptides. Df GnRH-ir cells and fibers were localized in the ganglia of the
terminal nerve and throughout the ventro-caudal telencephalon and preoptic area.
These cells project to hypothalamic areas, centers of sensory and behavioral
integration in the diencephalon, and the midbrain. A large, discrete cII GnRH-ir
cell nucleus was found in the midbrain tegmentum. CII GnRH-ir fibers project to
the hypothalamus and regions of the pituitary, but were more concentrated in
sensory processing centers in the midbrain and hindbrain than the df form. This
is the first study to show differential distribution of cII and df GnRH in the
elasmobranch brain, and supports the hypothesis of divergent function of GnRH
variants such as gonadotropin control and neuromodulation of sensory function.
Stephen
M. Kajiura (MS Biology 1994)
Seasonal dynamics of dental sexual dimorphism in the Atlantic stingray, Dasyatis
sabina (Lesueur) 1824
Abstract: The reproductive mode for all elasmobranch
fishes involves internal fertilization which is rare in fishes. Copulation
requires prolonged contact between the sexes and is facilitated by males biting
their female mates. The teeth of most male batoids are known to be pointed while
female teeth are generally rounded, but there are no known differences in food
habits among the sexes that can account for this phenomenon. It was hypothesized
that the pointed dentition of males evolved to increase reproductive success by
providing a firm grip on females during copulation. Dentition of the Atlantic
stingray, Dasyatis sabina, was examined from fish sampled over 24
consecutive months. Digitized images of the teeth were used to quantify tooth
morphology. Male tooth shape was characterized by a pointed cusp during the
mating season but was replaced by a molariform crest during the non-mating
season. In contrast, female teeth were molariform throughout the year.
Furthermore, tooth replacement rate did not differ between the sexes which
indicates that molariform teeth are not a result of differential wear. Females
also exhibit a thicker dermis that males, during both the mating and non-mating
seasons, which probably serves to minimize damage to underlying tissue. This
work is the first to demonstrate seasonal changes in tooth morphology that
coincides with reproductive activity. Thus the phenotypic plasticity in tooth
shape in male batoids is a cyclic phenomenon driven by selection for mating
rather that feeding efficiency.
Toko
Fujita (BA Biology 2004)
My research goal in the lab was to examine the function of gonadotropin-releasing hormone (GnRH) variants in the brain of coral reef fishes. GnRH is widely known for its role in reproduction. However, immunocytochemistry experiments show distinct distributions of GnRH in areas of the brain involved in sensory processing. One of the ways to study the function of GnRH in these sensory regions is to determine whether specific GnRH receptors are also located in these regions. I used molecular techniques to identify the gene sequence for GnRH receptors in the saddle back wrasse (Thalassoma duperrey).
Karen
P. Maruska (MS Biology 1996)
Ecological morphology of the peripheral mechanosensory lateral line in the
Atlantic stingray, Dasyatis sabina
Abstract: The mechanosensory lateral line system in teleosts functions in prey detection, but the peripheral organization and ecological functions in elasmobranch fishes are unknown. This study examined the anatomy, spatial organization and innervation patterns of lateral line mechanoreceptors in the Atlantic stingray (Dasyatis sabina) with emphasis on function in the localization and capture of natural prey. Sensory neuromasts of different morphological types are organized to maximize the detection of mechanoreceptive stimuli. Superficial neuromasts (SN) are arranged in bilateral rows along the dorsal midline from the spiracle to the tip of the tail and are oriented to detect water stimuli in the transverse plane. The dorsal canals consist of the interconnected hyomandibular (HYO), infraorbital (IO), supraorbital (SO), and posterior lateral line (PLL) subsystems composed of main canals that bear sensory neuromasts and extensive neuromast-free lateral tubules that extend the receptive fields towards the disc margin. The ventral canals consist of the HYO, IO, SO and also the short separate mandibular (MAN) located on the lower jaw. An extensive, confluent and compliant ventral inner canal system lacks surface pores and extends rostrally from the pelvic region to the head where it expands between the mouth and disc margin. Vesicles of Savi (VS) are located in bilateral rows on the ventral midline of the snout and each is distinguished by three juxtaposed neuromasts within an isolated subdermal pouch. Across adult size classes (22 - 32 cm disc width) the number of canal neuromasts on the body increase only in the MAN and dorsal SO canals but show no increase in the number of axons per neuromast. Single unit extracellular recordings from canal primary afferent fibers show both regular (70% of recorded fibers) and irregular (30%) resting discharge patterns. Superficial neuromasts were innervated only by regular fibers. Further, fibers that innervate neuromasts in the ventral non-pored canal system only responded to touch of the skin over the canal. It is hypothesized that 1) superficial neuromasts detect transverse water flow across the body caused by tidal currents, conspecifics, or predators, 2) pored ventral canals detect water motion made by prey near the disc margin, and 3) non-pored canals and vesicles of Savi require direct contact of prey with the skin and function as touch receptors to guide exposed prey towards the mouth.
Karen P. Maruska (PhD Zoology 2007)
Acoustic communication, auditory processing and neuropeptide modulation of sensory systems in coral reef fishes
Assessment of the underwater sensory environment is critical to the survival and reproductive success of fishes. Detection of sound stimuli is especially important both for assessing the general underwater auditory scene, and for acoustic communication during social interactions. The neural centers for processing of auditory information are subject to modulation by neurochemicals such as the neuropeptides gonadotropin-releasing hormone (GnRH) and arginine vasotocin (AVT).
The extensive non-hypophysiotropic projections of GnRH and AVT suggest they may function as neuromodulators of sensory and sensorimotor processing to mediate behaviors. This dissertation examines aspects of the acoustic communication and auditory processing abilities of the sound-producing Hawaiian sergeant damselfish, and tests several predictions of the sensory neuromodulation hypothesis, which states that GnRH and AVT can influence the processing of sensory information prior to integration with motor control circuits.
Hawaiian sergeant fish produce low frequency, low intensity sounds during close range agonistic, nest preparation, and courtship behaviors. The spectral characteristics of these sounds match the frequency range of hearing, as predicted by the acoustic communication hypothesis. This spectral match is supported by physiological data obtained by auditory evoked potentials, and single cell recordings from both the hindbrain and midbrain. Single cell recordings from auditory neurons in the hindbrain and midbrain in response to complex conspecific stimuli also show that the temporal information of the pulsed sounds produced by this species is represented in the auditory brain. These data provide support for the coevolution of sender and receiver physiologies to maximize detectability of biologically relevant acoustic signals in the Hawaiian damselfish.
Octavolateralis nerves in the Hawaiian sergeant fish terminate ipsilaterally within seven first order medullary nuclei: caudal (CON) and medial (MON) octavolateralis nuclei, anterior (AON), descending (DON), magnocellular (MgON), tangential (TON), and posterior (PON) octaval nuclei, and the eminentia granularis (EG) of the cerebellum. These octavolateralis projection patterns are most similar to the other perciform fishes examined, such as the oscar and sleeper goby. This study provides needed comparative data on octavolateralis projections and organization of medullary nuclei in a vocal perciform fish without specialized peripheral auditory structures.
Midbrain and hindbrain auditory neurons in the Hawaiian sergeant fish are either silent or have slow irregular resting discharges, and high phase locking ability. Best frequencies ranged from 80-400 Hz, but the majority of neurons were most sensitive to 100 Hz tone pips, which matches the spectral characteristics of natural sounds produced in the wild. Midbrain and hindbrain auditory neurons were also modulated by playbacks of complex natural conspecific sounds with mean thresholds similar to that at 100 Hz for tone pips, but lower than that at all other frequencies. These data on the response properties of the torus semicircularis and octaval nuclei in the hindbrain demonstrate that both the spectral and temporal components of the pulsed natural sounds produced by the Hawaiian sergeant fish are represented in the auditory brain.
Predictions of the sensory neuromodulation hypothesis were tested for both the visual system, and the lateral line and auditory systems. GnRH and GnRH receptors were localized in the retina and visual brain of four different perciform reef fishes. Thus, GnRH may modulate visual processing at multiple levels. These data provide neuroanatomical support for the sensory neuromodulation hypothesis, and indicate GnRH modulation of visual processing may be a conserved trait among vertebrates.
The GnRH somata in the non-hypophysiotropic regions of the terminal nerve and midbrain tegmentum showed sex and seasonal plasticity in number and size in the adult Hawaiian sergeant fish brain. These sex and seasonal variations were correlated with changes in GnRH-immunoreactive (-ir) fiber densities in the sensory torus semicircularis, tectum and vagal lobe. Varicose GnRH-ir axons were also found closely associated with individual auditory neurons in most hindbrain octaval nuclei. These results provide neuroanatomical support for the sensory neuromodulation hypothesis that GnRH can modulate octavolateralis sensory processing at multiple levels within the brain.
Sex and seasonal plasticity in AVT somata number and size was also observed within all three AVT-ir cell groups (pPOA, mPOA, gPOA). AVT-ir fiber densities in the torus semicircularis and vagal motor nucleus also varied seasonally and were most correlated with temporal changes in the number of gPOA somata. These results provide neuroanatomical support for the hypothesis that AVT can modulate octavolateralis sensory and sensorimotor processing at multiple levels within the brain.
Preliminary neuromodulation experiments indicate that GnRH has an inhibitory effect on auditory neurons in the torus semicircularis of the damselfish brain, evident by a GnRH-induced decrease in spike rate compared to saline controls. Inhibitory effects of GnRH are common in various neuron types, but the biological significance of this response requires further testing. Nevertheless, these preliminary experiments provide some physiological evidence that GnRH can influence the processing of auditory information in the fish brain.
The data presented in this dissertation provide support for the acoustic communication hypothesis in the Hawaiian sergeant fish, and support for the sensory neuromodulation hypothesis that GnRH and AVT have the potential to influence octavolateralis processing in the fish brain.
Mindy Mizobe (BS Zoology 2007)
Neuropeptide distribtion in reef fish
I studied the seasonal distribution of AVT and GnRH in the brain of the bluespot goby.
Courtney
R. Lowrance (MS Biology 1999)
The development of the mechanosensory and electrosensory lateral line : a model of sensitivity and resolution
Ariel C. Rivera-Vicente MS Zoology 2007)
Spatial model of the electrosensory array in the scalloped hammerhead shark, Sphyrna lewini
I studied the neural processing of uniform electric fields by sharks and rays. The sensory biology and behavior used in the detection of small polar electric fields by elasmobranchs during feeding and mating are well known. In contrast, several theoretical models exist for the use of the electrosense to detect geomagnetically induced electric fields. My research focused on the peripheral organization of the electrosensory system of the hammerhead shark. A spatial model of spatial projections was determined from detailed dissections of of individual canals grouped by cluster. This provided a morphological basis for future investigations on the functional subunit hypothesis.
Josiah
Sewell (MS Zoology 2007)
Functional morphology of the electrosensory system in the brown stingray (Dasyatis
lata)
I studied the spatial projections of ampullary arrays in the brown stingray. This species has very long and sensitive canals with projections primarily in the horizontal plane.
Joseph
A. Sisneros (PhD Biology 1999)
Ontogenetic and androgen-induced changes in the response properties and
function of the elasmobranch electrosensory system
Abstract: All elasmobranch
fishes possess a single class of electroreceptors known as the ampullae of
Lorenzini. The ampullary electroreceptor system is an important sensory system
used for prey detection, orientation, and social communication. No
previous study has addressed the function of the elasmobranch electric sense in
pre-adult stages or during periodic reproductive cycles as adults. The aims of
this study were to determine if the response properties and functions of the
elasmobranch electric sense change during ontogenetic development and during
annual periods associated with different levels of serum androgen in adult male
elasmobranchs. I test the hypothesis that dihydrotestosterone (DHT) modulates
the annual periodic changes in the response properties of the elasmobranch
electrosensory system and that androgen receptors are expressed in ampullary
electroreceptors.
The response properties of electrosensory primary afferent
neurons of pre-hatch embryo (8-11 week), post-hatch juvenile (1-8 month), and
adult (>2 yr.) clearnose skates (Raja eglanteria) were examined to
determine whether encoding of electrosensory information changes with age, and
if the electric sense is adapted to encode natural bioelectric stimuli across
life history stages. During ontogeny, electrosensory primary afferents
increase resting discharge rates, spike regularity, and sensitivity at best
frequency. Best frequency was at 1-2 Hz for embryos, showed an upwards
shift to 5 Hz in juveniles, and a downward shift to 2-3 Hz in adults.
Encapsulated embryos exhibit ventilatory movements that are interrupted by a
"freeze response" when presented with weak uniform fields at 0.5 and 1
Hz. This phasic electric stimulus contains spectral information found in
potentials produced by natural fish predators, and therefore indicates that the
embryo electrosense can efficiently mediate predator detection and avoidance.
In contrast, reproductively active adult clearnose skates discharge their
electric organs at rates near the peak frequency sensitivity of the adult
electrosensory system, and therefore facilitates electric communication during
social behavior.
In the adult Atlantic stingray, Dasyatis sabina, the
androgen DHT shows a distinct pattern of annual cycling associated with the
reproductive season. During the period of primary androgen production at
the onset of the mating season, electrosensory primary afferent neurons decrease
discharge variability, show a downward shift in best frequency (BF) and an
increase in the low frequency bandpass. To test the hypothesis that
androgens cause the change in the frequency response properties, adult male rays
were collected during the non-reproductive season and implanted with DHT.
Ten to fourteen days after implantation, DHT treated rays had lower BFs and a
lower bandpass than controls. In addition, DHT treatment increased the
sensitivity of primary afferents to low frequency electric stimuli (0.25-5 Hz)
by a factor of 1.6x compared to that observed in controls. Results form
immunocytochemistry and Western blot experiments confirm that androgen receptors
are differentially expressed in the ampullary electroreceptors during the mating
and non-mating seasons. Androgen receptors in ampullary electroreceptors
are up-regulated at the onset of the mating season during primary androgen
production in adult male stingrays.
These results lead me to suggest that life history-dependent
functions may shape the evolution of the low frequency response properties for
the elasmobranch electrosensory system. In addition, androgen-induced
changes in the frequency response properties of ampullary primary afferents that
occur in male elasmobranchs at the onset of mating activity may represent an
adaptation to enhance mate detection and increase reproductive fitness during
the mating season.
Brook
Swanson (BA Biology 1998)
My research in the lab focused on the second order processing of electrosensory information in the brain of Dasyatis sabina. This research has included response properties of the principal cells of the dorsal octavolateralis nucleus (DON) conducted using glass microelectrodes and a range of stimulus intensities and frequencies. I examined the effects of Gn-RH peptides on system function by micro-injections of the peptide while conducting extra cellular recordings with multi-barrel micro-electrodes. The recorded data were analyzed using Spike 2 software to find thresholds of response and changes in response parameters. This research will further the understanding of the processing of ecologically significant electrical stimuli in the elasmobranch brain.
Jonathan
Trumbull (Electrical Engineering 1996)
Ultrasonic Neural Transmitter
The
ability of elasmobranchs to detect electric fields (current flows) in water was
discovered and quantified through behavioral studies. Some of the underlying
mechanisms of this sensory modality have also been characterized using standard
neural recording techniques in bench experiments. My work stems from the desire
to obtain real-time neural information in free swimming elasmobranchs. The model
animal used for our experiments has been everyone's favorite fish: the stingray.
After lightly anesthetizing the animal, a custom fabricated silicon electrode
(developed for Dr. Tricas' Lab by the University of Michigan) is inserted
through the cranial cavity into the dorsal octavolateral nucleus (a hindbrain
region located below the cerebellum). This is the site where electrosensory
information is first processed. After locating and isolating the cell body of a
second order neuron, the animal is allowed to recover and released. The
electrode leads to an amplifier/transmitter module mounted on the animal's back.
This sealed, battery-powered module boosts the neural signal (action potential)
to a detectable level. Then for each action potential detected, the transmitter
sends a pulse of ultrasonic energy through the water. This pulse is detected and
recorded using a hydrophone and an analog data recorder. By correlating the
neural discharge profile with a video of the swimming path through a known
electric field, valuable information can be obtained about how the animal
actually localizes and obtains information about field sources.