STUDY OF NEUROSECRETORY CELLS IN ODONATA

Aishwarya D. Atilkar, Suresh C Masram

Post graduate teaching department of zoology, Nagpur University
Rashtrasant Tukadoji Maharaj Nagpur University, Amravati Rd,
Nagpur, Maharashtra India 440033
Email : aishatilkar@gmail.com

ABSTRACT
The intricate neurosecretory processes in Odonata species, particularly dragonflies, reveal the
cyclic pattern of secretory activity in the last instar larva's developmental stage. Neurohormones
released by medial neurosecretory cells play a pivotal role in orchestrating metamorphosis,
highlighting the complexity of dragonfly neural structures. Treatment with Protocerebral medulla
affects the corpora cardiaca, emphasizing its role as a neurohaemal organ storing neurosecretory
material. The study of descending contralateral movement detectors and target-selective
descending neurons unveils insights into dragonflies' prey detection and pursuit mechanisms.
Neurosecretory cells in the ventral ganglia exhibit diverse types, paralleling those in the brain,
indicating shared roles in physiological regulation. The corpora allata's dual states in hormonal
regulation and distinctive features of neurosecretory cells contribute to the understanding of
dragonfly hormonal and neural complexities. Investigations into dragonfly olfactory capabilities,
larval head anatomy, and neuropeptide amidation shed light on sensory adaptations and
biochemical defense mechanisms. The abstract concludes with a focus on neurohormones' varied
roles, from regulating Malpighian tubules to influencing sugar levels, emphasizing their crucial
involvement in maintaining insect physiological balance.
Introduction dragonfly Orthetrum Chrysis the
histomorphology of the cephalic
The nervous and endocrine systems work
neuroendocrine system in the ultimate
hand in hand in a process known as
instar larva and the adult (Highnam,
neuroendocrine integration together, they
1969; Wigglesworth, 1970).
play a crucial role in regulating various
Since the initial documentation by
physiological functions, ensuring the
day in 1940, extensive research has been
overall balance of the body, and
conducted by numerous scholars on the
responding swiftly to stress this
neurosecretory cells (NSC) located in the
collaborative effort is essential for
ventral ganglia of various insects
maintaining both everyday internal
however, the majority of earlier
stability and a rapid reaction to
investigations were limited to the NSC
challenging situations (Hartenstein, 2006;
found in the subesophageal ganglion
Adamski et al. 2019).
more recently, there has been a shift
A perusal of the ever-growing study of towards more comprehensive
the neuroendocrine system of insects has examinations, providing detailed insights
reveals that little work has been done on into the cytomorphology, classification,
Odonata in comparison to other and distribution of NSC in not only the
orders,present investigation has, suboesophageal ganglion but also in the
therefore, been undertaken to study the thoracic and abdominal ganglia (Scharrer,
structure and physiological activities of 1941; Arvy, 1952).
the neuroendocrine system in the Researchers have investigated
neurosecretory cells (NSC) in Odonata,
particularly focusing on nymphs of
certain dragonflies one notable study
focus into the NSC not only in the
subesophageal ganglion but also
extends the exploration to encompass
the thoracic and abdominal ganglia of
nymphs belonging to the Aeschna
grandis species this study contributes
to our understanding of the distribution
and characteristics of NSC in different
parts of the nervous system among
dragonfly nymphs (Charlet, 1969).
Until now, there has been a noticeable
gap in research focusing on adult
dragonflies study aims to shed light on
the intricacies of the structure and function
of the neurosecretory system located in the
ventral ganglia of adult dragonflies, with a
specific focus on the species Orthetrum
chrysis the neurosecretory mechanisms
operating in the adult stage of this
particular dragonfly species.
Histological studies and classifications
of neurosecretory cells in dragonflies
reveal there is a notable absence of
information regarding the nature of these
cells specifically, there is no account of
whether they exhibit different phases of
activity within a single cell or if they
vary from one another in their nervous
system modules (NSM) , To address this
gap, the current study was initiated with
the aim of determining the nature of
neurosecretory cells in Orthetrum
Chrysis ( Schaller, 1968; Charlet, 1972).
The initial examination of the
endocrine glands in Odonata, appears to
have been inaccurate in terms of the
spatial arrangement of these organs.
Baldus was the first to describe the nervi
corporum cardiacarum Interni (NCCI)
and their connection with the
"stomatogastric ganglia" (corpora
cardiaca) however, he did not recognize
their functional significance.
Furthermore, Baldus provided an
account of the protocephalic
neurosecretory system in various
Odonata but couldn't find any indication
of the nervi corporum cardi-Acarum
externi (NCCII). He also struggled to
locate the nervi corporum allatarum
(NCA) in nymphs it was reported that a
delicate pair of nerves, the NCCII, ran
from the brain to the corpora cardiaca.
Interestingly, it is found that these
nerves are present only in mature
nymphs and adults. Additionally, Cazal
asserted the presence of nervi corporum
allatarum (NCA) in mature nymphs this
information highlights the evolving
understanding of the neuroendocrine
system in Odonata over different studies
and time periods.
Brain
In the Odonata species, the
neurosecretory cells within the brain
showcase a cyclic pattern of secretory
activity during the developmental stage
of the last instar larva notably , the
neurohormones released by the medial
neurosecretory cells play a
predominant role in orchestrating the
metamorphosis of the larva into a fully
developed adult dragonfly this
information underscores the
remarkable complexity of the neural
structures in dragonflies and sheds
light on the crucial role played by
neurosecretory cells and associated
neurohormones in the intricate process of
metamorphosis from larva to adult
(Schaller, 1959; 1970).
Larvae are treated with PME
(Protocerebral medulla), the corpora
cardiaca, which is a part of the insect's
brain, doesn't show any detectable
neurosecretory material this is because
the corpora cardiaca functions as a
neurohaemal organ, meaning it stores the
neurosecretory material produced by
specific cells in the brain , In other
words, instead of producing the material
itself, the corpora cardiaca acts like a
storage facility for these important
substances that play a role in various
physiological processes in the insect
brain (Tembhare, 1976).
Larvae are treated with PME
(Protocerebral medulla), it reduces the
secretion activity of the special cells
within the corpora cardiaca in simpler
terms , PME treatment decreases the
ability of specific cells in the insect's
brain to release important substances
stored in the corpora cardiaca , this could
have implications for various
physiological functions in the insect, as
these substances play a role in regulating
different processes within the body
(Varadaraj et al. 1993). The electrical
activity of neurons responsible for
detecting prey, specifically those
involved in recognizing downward
movement on the opposite side (known
as descending contralateral movement
detectors or DCMDs), is being studied in
the brain. In simpler terms, scientists are
examining how certain brain cells
respond to and process information
about the downward movement of
potential prey understanding the
electrophysiological behavior of these
neurons can provide insights into the
mechanisms underlying the insect's
ability to detect and react to specific
types of movement in its environment
(Gonka et al.1999).
Neurons in the dragonfly brain known as
target-selective descending neurons
(TSDNs). In simpler terms, scientists are
studying specific cells in the dragonfly's
brain that play a role in selecting and
responding to particular targets these
neurons are involved in the dragonfly's
ability to focus on and pursue specific
objects or prey, Studying the behavior of
target-selective descending neurons
helps us understand how dragonflies
process information and navigate their
surroundings to capture their intended
targets (Frye, 1995).
In the dragonfly species Orthetrum
Chrysis, there are cells known as type B
and C cells located in the optic lobes of
their brains these cells contain a
substance that reacts positively to PF
staining it was observed specific cells in
the dragonfly's optic lobes and these cells
, labeled as type B and C, show a positive
reaction to a staining technique called PF
staining this staining indicates the
presence of certain materials in these
cells, Investigating these cells and the
substances they contain helps researchers
better understand the structure and
function of the dragonfly's visual
processing system ( Benedeczky. L et al.
1982 ). In the brain region called the pars
intercerebralis of the dragonfly
Orthetrum Chrysis , there are three types
of cells known as A, B, and C cells these
cells are distinct from each other and are
responsible for producing different types
of neurosecretory material (NSM) to put
it simply, in a specific part of the
dragonfly's brain , there are three
different types of cells, labeled A, B, and
C, and each of these cells produces a
unique chemical substance that plays a
role in the insect's nervous system
investigating these distinct cell types
helps scientists understand the diversity
of functions within the dragonfly's brain
(Tembhare et al. 1975).
In dragonflies and damselflies (odonates),
the corpora allata, which are glands
involved in hormonal regulation, have
two different states these glands are
actively producing hormones, they are in
a syncytial condition, meaning their cells
are fused together without clear
boundaries on the other hand , when the
corpora allata are not actively producing
hormones, they are in a cellular state with
distinct cell walls separating individual
cells these glands in these insects have
two forms: one where the cells are fused
together during hormone production, and
another where the cells are separate when
the gland is not actively engaged in
hormone secretion this distinction in the
structure of the corpora allata is essential
for understanding the hormonal
regulation processes in dragonflies and
damselflies (Schaller et al. 1970;
Tembhare et al. 1994).
Neurosecretory cells
In the ventral ganglia of insects,
specifically in the lower part of their
nervous system, there are cells known as
neurosecretory cells similar to the brain
cells, these ventral ganglia cells come in
various types, and scientists classify them
based on their preferences for different
stains, as well as their size and location in
the ganglia this classification was
established by (Raabe, 1971). The A, B,
C1, and C2 cells in the ventral ganglia
are specifically examined in terms of
their neurosecretory nature, meaning
their ability to release substances that
play a role in the nervous system the fact
that these cells produce chemically
different nervous system modules (NSM)
provides strong support for categorizing
them into distinct types of specific cells
in the lower part of the insect nervous
system, and by studying their staining
properties, size, and location, they have
found evidence supporting the idea that
these cells function differently in terms of
the substances they produce for the
nervous system (Thakare et al. 1975).
The neurosecretory cells (NSC) found in
the ventral ganglia of insects have
similarities to those located in the Pars
intercerebralis region of the brain in
Orthetrum chrysis, these cells responsible
for releasing substances in the lower part
of the insect's nervous system are
comparable to the cells found in a
specific area of the brain in Orthetrum
chrysis this suggests that there are
common features or functions between
these two sets of cells, potentially
indicating shared roles in the regulation
of the insect's physiological processes,
Studying these similarities helps
scientists understand how different parts
of the insect's nervous system work
together to control various functions in its
body (Thakare et al. 1977).
Cells labeled as A and B are considered
genuine neurosecretory cells, meaning
they truly release substances that play a
role in the nervous system on the other
hand, cells labeled as C are categorized as
false neurosecretory cells, indicating that
they don't actually release these substances
cells A and B, they actively contribute to
the release of important substances in the
nervous system however, these cells
labeled as C, they may resemble
neurosecretory cells but don't function in
the same way; they don't release the
substances associated with nervous system
regulation this distinction helps researchers
understand the different types of cells and
their roles in the intricate functions of the
nervous system (Highnam, 1961).
The B cells are identified as genuine
neurosecretory cells because they contain
certain chemical groups, specifically SH
(sulfhydryl) and SS (disulfide) groups and
confirmed that B cells are indeed
neurosecretory cells by detecting the
presence of specific chemical groups
within them these groups, SH and SS, are
indicative of the cell's ability to release
substances involved in nervous system
functions, this identification is crucial in
understanding the role of B cells in the
intricate processes of the nervous system
(Chalaye, 1967).
In the anterodorsal region of the medial
part of the pars intercerebralis medialis,
there are two sets of neurosecretory cells
located on either side of the root of the
Medial ocellar nerve these neurosecretory
cells into three categories, labeled as A, B,
and C, based on specific criteria this
classification was established by various
scientists, including Nayar (1955),
Johansson (1958), Highnam (1961), and
others, a particular area of the insect brain,
there are cells that release substances
important for the nervous system.
Scientists have observed these cells on
either side of a nerve root and have sorted
them into three groups (A, B, and C) using
certain criteria set by researchers like
Nayar, Johansson, Highnam, and others
this classification helps in understanding
the diversity and functions of these
neurosecretory cells in the insect brain
(Nayar, 1955; Johansson, 1958; Highnam,
1961; grillot, 1971).
Neuroendocrine system
Considerable information has been gathered
regarding the MNC (Methyl Naphthyl
Ketone)
groups in various other species of
dragonflies, MNC groups in dragonflies
beyond the specific
species initially mentioned this accumulated
knowledge contributes to a broader
understanding of how MNC groups function
across diverse dragonfly species, shedding
light on their
ecological roles, behavioral patterns, or any
unique features they may exhibit in different
contexts this wealth of information aids
researchers in comprehensively studying and
comparing
the roles and behaviors of MNC groups
across the broader spectrum of dragonfly
species
(Hanstrom, 1940).
The natural peptide antigens found in the
stained neurons could be a part of either the
pancreatic polypeptide family or the FMR
Famide family to delve deeper, when
examining
stained neurons, scientists have identified
endogenous peptide antigens these particular
peptides,
or protein fragments, might be associated
with two distinct families: the pancreatic
polypeptide
family or the FMR Famide family these
families are groups of related peptides with
specific
structures and functions, Investigating the
presence of these peptide antigens in neurons
provides
valuable information about the potential
involvement of these peptide families in
neural
processes, offering insights into the complex
molecular dynamics within the nervous
system
(White et al.1986).
The regulation of ionic balance through
hormones seems primarily associated with
the
neurohormones produced by A cells,
However in certain insects, the cells of the
Pars
intercerebralis in the brain also play a role
the intricate system of hormonal regulation
that
maintains the balance of ions within an
organism appears to have a primary player in
the form
of neurohormones from A cells these
neurohormones likely orchestrate the
physiological
processes involved in ionic balance notably,
in specific insects, an additional regulatory
component comes into play – the cells of the
Pars intercerebralis located in the brain these
cells
likely contribute to the overall control of
ionic balance, showcasing the complexity
and
variation in hormonal regulatory mechanisms
across different insect species of brain
(Berridge,
1966; Vietinghoff, 1966; Wall, 1967; Mills,
1967; Pilcher, 1970).
In B cell Geminata, A-cells exhibit active
synthesis and secretion of neurohormones
but in
PME treated larvae, the Cells gradually stop
their secretory activity technics and radio
immunoassays of extracts from the brain,
several gastro-entero-pancreatic hormones
and
neuropeptides have previously been detected
in the insect nervous system, e.g. :
cholecystokinin/gastrin (Dockray. J. G, 1981;
Duve. H, 1982; El-Salhy. M, 1980).
Despite the absence of fully developed
olfactory glomeruli, the dragonfly species L.
depressa
demonstrates the ability to sense olfactory
stimuli, as evidenced by electrophysiological
recordings L. depressa lacks fully mature
olfactory glomeruli, which are specialized
structures in the brain associated with the
sense of smell, the dragonfly displays
proficiency in detecting
olfactory stimuli this capability has been
observed and confirmed through the use of
electrophysiological recordings, a method
that involves measuring electrical
activity in response to sensory stimuli the
findings suggest that L. depressa employs
alternative
or less conventional mechanisms to perceive
and respond to olfactory cues, highlighting
the
adaptability and complexity of sensory
processes in this particular dragonfly species
(Rebora et
al. 2012).
Distinctive features known as olfactory
glomeruli are characteristic elements found
in
the primary olfactory centers of both
vertebrates and advanced invertebrates the
olfactory
glomeruli are specialized structures found in
the brains of vertebrates and certain higher
invertebrates, serving as crucial components
of their primary olfactory processing centers
these
structures play a key role in the initial stages
of olfaction, where sensory information
related to
smell is received, integrated, and processed
the presence of olfactory glomeruli
associated with
the sense of smell in both vertebrate and
advanced invertebrate species (Hildebrand et
al. 1997;
Joseph, 2020).
The internal head anatomy of Epiophlebia in
its larval stage is severely incomplete and
lacking in detailed information while
examining the internal structures of the head
in the larval
phase of Epiophlebia, researchers have
encountered significant challenges due to the
fragmentary nature of the available
information the limited details hinder a
comprehensive
understanding of the larval internal head
anatomy of this particular species this gap in
knowledge
underscores the need for further research and
exploration to fill in the missing pieces and
gain a
more thorough insight into the intricacies of
Epiophlebia's larval head anatomy (Asahina,
1954;
Tramu. G et al.1983). Lead ions being
effective in this connection could only be
present In very
low concentrations in the hemolymph fluid,
which normally is separated from The brain
tissue
by a neural lamellar sheath as an effective
barrier against uncontrolled Ion influx
(Treheme,
1972).
Numerous neuropeptides undergo a process
known as amidation at their C-terminus this
biochemical modification serves a crucial
purpose – it effectively shields the free
carboxyl
group present at the end of the peptide chain
the rationale behind this protective measure
lies
in preventing swift and indiscriminate
degradation by carboxypeptidases when
these
neuropeptides are circulating in the
bloodstream to elaborate, amidation involves
the
conversion of the terminal carboxyl group
into an amide, a more stable chemical
structure this
alteration is akin to placing a molecular
guard on the vulnerable end of the
neuropeptide, shielding it from enzymatic
attacks that could otherwise break it down
too rapidly In the
dynamic environment of the bloodstream,
where various enzymes are at play, this
amidation at
the C-terminus acts as a strategic defense
mechanism, ensuring the neuropeptides
maintain
their structural integrity and functionality
until they reach their intended targets or
undergo
regulated degradation (Goldsworthy et al.
1989).
In the developmental stage of the dragonfly
species Tramea virginia, specific cells known
as A-cells play a vital role these A-cells
release a hormone called allatotrophic
neurohormone,
which serves to activate the corpora-allata,
and another hormone called
prothoracicotropic
neurohormone, which stimulates the ventral
glands this intricate hormonal signaling
system
plays a crucial part in regulating various
physiological processes during the larval
stage of
Tramea virginia (Tembhare et al. 1994).
Neurohormones, which are signaling
molecules in the nervous system, play a role
in
regulating the Malpighian tubules,
specialized structures involved in excretion
in insects and
other arthropods when these neurohormones
act on the tubules, they prompt a rapid
release of
fluid from the hemolymph, the insect's
circulatory fluid this heightened fluid
movement leads to
an intensified diuretic response, where the
insect expels a notably increased volume of
urine this
physiological process is essential for
maintaining the insect's internal balance of
fluids and waste
products (Highnam, 1969; Cazal, 1947;
Mordue, 1969).
The intrinsic cells responsible for regulating
the sugar levels in the hemolymph of
dragonfly
larvae do not produce neurohormones these
intrinsic cells, which are integral to
maintaining the
appropriate sugar concentration in the
hemolymph (the circulatory fluid of the
larva), do not
engage in the production of neurohormones
these are signaling molecules that typically
play a
role in the control and coordination of
physiological processes in the absence of
neurohormone
production by these intrinsic cells suggests
that other mechanisms or factors may be at
play in
the regulation of hemolymph sugar levels in
dragonfly larvae physiology remains a
subject of
interest and investigation in understanding
the intricacies of metabolic control in these
developmental stages (Tembhare et al.
1991c).
Neurohormones, which are active substances
made of proteins, are created and released
by regular neurons to elaborate, neurons, the
fundamental cells of the nervous system,
have
the capacity to produce and release
neurohormones these neurohormones, being
protein-based,
serve as signaling molecules that play
important roles in transmitting messages
within the
nervous system and often have widespread
effects on various physiological processes
the
synthesis and release of neurohormones by
neurons are essential aspects of the intricate
communication network that enables the
nervous system to regulate and coordinate
activities
throughout the body (Bern, 1962; Scharrer,
1969; Wigglesworth, 1970).
Neurohormones, regardless of their origin,
play a crucial role in maintaining the balance
of
water and electrolytes in insects
neurohormones are key players in the
regulation of water and
electrolyte levels within the bodies of insects,
Regardless of where these neurohormones
come
from, whether it's the nervous system, certain
glands, or other sources, their primary
function is
to orchestrate processes that ensure a stable
internal environment for the insect this
includes
controlling the absorption and excretion of
water and electrolytes, crucial factors for the
insect's
overall physiological well-being the intricate
involvement of neurohormones in these
processes
underscores their significance in
orchestrating the delicate balance of fluid
and electrolyte
homeostasis in insect physiology (Novak,
1975).
Conclusion
The adult dragonfly, Orthetrum chrysis,
exhibits a classification of neurosecretory
cells in its
ventral ganglia, denoted as A, B, C1, and C2
cells. These cells are identified based on
three
criteria: the presence of stainable granules,
the occurrence of neurosecretory material in
their
axons and terminals, and cyclic activity that
involves changes in the quantity of
neurosecretory material corresponding to
physiological activities. A neuroanatomical
study
has unveiled the existence of spherical knots
in the aglomerular antennal lobe, suggesting
a
potential role in the perception of odors.
Neurons believed to regulate interception in
dragonflies are accessible through tracts in
the third neuropil of the optic lobe. The
subesophageal ganglion (SEG), located
ventrally just below the brain and esophagus,
exhibits
the presence of immunoreactive deposits
within the insect neurohaemal organ. The
term
"cephalic endocrine glands" encompasses
various structures, including neurosecretory
cells of
the pars intercerebralis and their axons,
corpora cardiaca, corpora allata, and ventral
glands.
The physiology of neurons accessible
through tracts in the third neuropil of the
optic lobe,
and the neurosecretory axons, likely
corresponds to those immunohistochemically
detected.
Interestingly, the removal of the pars
intercerebralis region of the brain and
ligature at the
neck region do not provide any indication of
involvement of hormones from the brain and
other endocrine organs of the cephalic
region. Flight muscles, which oscillate under
direct
flight control, exhibit one-to-one matches
between neuronal stimulus. Notably, in both
adult
and nymphal dragonflies, the same brain
regions seem capable of processing highly
diverging
information from different sensory
structures. This intricate network of
neurosecretory cells,
anatomical structures, and physiological
processes underscores the complexity and
adaptability of the dragonfly's nervous and
endocrine systems.
Reference
Asahina. S (1954). A morphological
study of a relic dragonfly
Epiophlebiasuperstes Selys
(Odonata, Anisozygoptera). Tokyo:The
Japan Society for the Promotion of Science.
Adamski, Z., Bufo, S. A.,
Chowański, S et al. (2019). Beetles as
model organisms in
physiological, biomedical and environmental
studies Frontiers in Physiology, 10: 319.
Arvy, Gabe (1952).
Histophysiological data on the retrocerebral
endocrine formations of
some Odonates Annaels Des Sciences.
Natural Zoology and Animal Biology 14:
345-374.
Baldus ( 1924). Studies on the
structure and function of the brain of the
larvae and imago
of dragonflies Natural Sciences 12 (15), 284-
285.
Bern. A. H (1962). The properties of
neurosecretory cells. General and
Comparative
Endocrinology, 1, 117-132.
Berridge. J. M (1966). The
physiology of excretion in the cotton-stainer,
Dysdercus fasciatus
Signoret. IV. Hormonal control of excretion.
Journal of Experimental Biology, 44, 553-
566.
Benedeczky. L, Kiss. L, Somogyi. P
(1982). Light and electron microscopic
localization of
substance P-like immunoreactivity in the
cerebral ganglion of locust with a
monoclonal
antibody. Histochemistry, 75, 123-131.
Charlet. M (1972). Histological study
of the pars intercerebralis of the larvae of
Aeschna
cyanea Mull. Reports of the Academy of
Sciences Paris, 275, 745-748.
Chalaye. D (1967). Neurosecretion at
the level of the ventral nerve chain of
Locusta
Migratoria migratorioides. “Bulletin of the
Zoological Society." 92: 87-108.
Cazal . P (1947). Research on the
retrocerebral endocrine glands of insects. II.
Odonates.
“Archives of Experimental and General
Zoology", 85: 55-82.
Duve. H, Thorpe. A (1981).
Gastrin/cholecystokinin (CCK)-like
Immunoreactive neurones
in the brain of the blowfly. General and
Comparative Endocrinology 43, 381-391.
Dockray.J, Duve.H,(1981).
Immunochemical characte-Rization of
gastrin/cholecystokinin-
like peptides in brain of Blowfly,General
Comparative Endocrinology 45, 491-496.
ElSalhy. M, Falkmer. S ,Grimelius. L
(1980). Immunohistochemical evidence of
gastro-
entero-pancreatic Neurohormonal peptides of
vertebrate type in the nervous system of the
Larva of a dipteran insect, the hoverfly,
Eristalisaenus. Regulatory Peptides, 187-204.
. Medical School, The University of Adelaide,
Frye. A. M, Olberg. M. M (1995).
Visual receptive field properties of feature
detecting
neurons in the dragonfly. Journal of
Comparative Physiology. A 177: 569-576.
Gonka. D. M, Laurie. J, Prete. R
(1999). Responses of Movement sensitive
descending
visual interneurons to prey-Like stimuli in
the praying mantis, Sphodromantislineola
"Brain,
Behavior, Evolution". 54: 243-262.
Goldsworthy. G, Mordue. W (1989).
Adipokinetic hormones: Functions and
structures.
Biological Bulletin , 177: 218-224.
Grillot. P, Provansal. A, Baudry. N,
Raabe (1971). The Perisympathetic Organs
of
Pterygote Insects: The Main Morphological
Types. Reports of the Academy of Sciences,
Paris.
Hartenstein. V (2006). The
neuroendocrine system of invertebrates: A
developmental
and evolutionary perspective. Journal of
Endocrinology. 190: 555–570.
Highnam. K.C (1961). The
Histology of the Neurosecretory System of
the Adult Female
Desert Locust, Schistocerca gregaria Journal
of Cell Science 3 (57), 27-38.
Highnam. K.C, Hill. L (1969). The
comparative endocrinology of the
invertebrates ,
Arnold, London.
Hildebrand. G. J, Shepherd. M. G
(1997). Mechanisms of Olfactory
Discrimination:
Converging Evidence for Common
Principles across Phyla. Annual Review of
Neuroscience.
Joseph. M, Basil. Jundi et al. (2020).
The complex optic lobe of dragonflies, 1
Adelaide
Adelaide, SA, Australia. 2 Biocenter,
Behavioral Physiology and Sociobiology,
University of Würzburg, Germany. 3
Department
of Biology, Londan University, Sweden. 4
Department of Neuroscience, Flinders
University,
Bedford Park, Australia.
Mills. R (1967). Hormonal control of
excretion in American cockroach. Release
ofdiure-
Tic hormone from the terminal ganglion,
Journal of Experimental Biology. 46: 35-41.
Nayar. K.K (1955). Studies on the
neurosecretory system of Iphita limbata Stal.
I.
Distribution and structure of the
neurosecretory cells of the nerve ring.
Biological Bulletin,
Marine Biology Laboratory, Woods Hole.
108: 296-307.
Novak. V. J (1975). Insect Hormones,
Chapman & Hall, London.
PilcherI. D. E (1970). Hormonal
control of the Malpighian tubules of the stick
insect,
Carausius morosus. Journal of Experimental
Biology, 52 : 653-665.
Raabe. M (1971). Neurosecretion in the
ventral nerve chain of insects and metameric
neurohemal organs. Archives of Zoology
Experimental Generalis, 112: 679-694.
Rebora. M, Salerno. G, PiersantiI. S
(2012). Olfaction in Dragonflies: An
electrophysiological evidence. Journal of
Insect Physiology, 58: 270–277.
Schaller. F, Charlet. M (1970).
Evolution of the neurosecretory system of
larva. Varadaraj.
A, Subramanian. S, Java. s (1993). Sublethal
effects of industrial effluents on the
biochemical
constituents of the haemolymph in the larva
of Macromia cingulata Rambur (Anisoptera:
Corduliidae). Odonatologica , 22: 89-92.
Schaller. F (1959). Weekly reports of the
sessions of the Academy of Sciences. 248:
2525.
Schaller. F, Meunier. J (1968). Study of
the head neurosecretory system of Odonata
insects. Bulletin de la Société Zoologique de
France, 93: 233-249.
Thakare. V. K, Tembhare. D. B (1975).
Histochemistry of the neurosecretory cells of
the
pars Intercerebralis of the dragonfly,
Orthetrum chrysis (Selys) (Anisoptera:
Libellulidae).
Odonatologica, 4:225-235.
Tembhare. D. B, Thakare. V. K (1977).
Neurosecretory System of the Ventral
Ganglia in
the Dragonfly, Orthetrum chrysis (Selys)
(Odonata: Libellulidae). Cell and Tissue
Research,
177:269-280.
Tembhare. D. B, Thakare. V. (1976). The
cephalic neuro-endocrine system of the
dragonfly Orthetrum chrysis (Selys)
(Anisoptera: Libellulidae). Odonatologica, 5:
355-370.
Tembhare. D. B, Andrew. R. J (1994).
Activity of the cephalic neuroendocrine
system
during the development of the last instar
larva of Tramea Virginia (Rambur)
(Anisoptera:
Libellulidae). Advances in Oriental
Odonatology. 34. Tembhare. D. B, Thakare.
V. K (1976).
The cephalic neuroendocrine system of the
dragonfly Orthetrum chrysis (Selys)
(Anisoptera:
Libellulidae). Odonatologica, 5: 335-340.
Tembhare. D. B, Andrew. R (1991a).
Hormonal influence on the haemolymph
trehalose
concentration in the dragonfly, Tramea
Virginia (Rambur) larva. 16: 165-166.
Tramu. G, Beauvillain. C, Pillez. J,
Mazzuca. M (1983). Presence of an
immunologically
apparent substance related to human
pancreatic growth hormone-releasing factor
(hpGRF) in
neurons of the hypothalamo-
hypophysiotropic area of guinea pigs and
rats. Reports of the
Academy of Sciences of Paris. 297: 435-440.
Treherne. J. E, Pichon. Y (1972). The
Insect Blood-Brain Barrier. Advances in
Insect
Physiology, 9: 253-313.
Wall. J (1967). Evidence for antidiuretic
control of rectal water absorption in the
cockroach, Periplaneta americana L. Journal
of Insect Physiology ,13: 565-578.
White. K, Hurteau. T, Punsal. P (1986).
Neuropeptide FMRF amide-like
immunoreactivity
in Drosophila: development and distribution.
Journal of Comparative Neurology, 247(4),
430-
538.
1
2
3