# A Review of the “Open” and “Closed” Circulatory Systems:  New Terminology for Complex Invertebrate Circulatory Systems in Light of Current Findings

Authors: Carl L. Reiber; Iain J. McGaw
Journal: International Journal of Zoology
 (2009)

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## Abstract

Invertebrate cardiovascular systems have historically been viewed as sluggish, poorly regulated, and “open”, where blood bathes the tissues directly as it moves through a system of ill-defined sinuses and/or lacunae without an endothelial boundary. When examining cardiovascular/circulatory morphology and physiology in a broader evolutionary context, one can question the very nature of the definition of a “closed” versus “open” circulatory system. Viewed in this context a number of invertebrates have evolved incomplete or even completely cell-lined vessels and or lacunae with a highly branched vasculature that allows for the production of significant driving pressures and flows to meet relatively high metabolic demands driven by active life styles. In light of our current understanding of invertebrate cardiovascular systems and their paralleled complexity to vertebrate systems, a number of long established paradigms must be questioned and new definitions presented to better align our understanding of the nature of “open” versus “closed” cardiovascular systems.


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## Body

## 1. Introduction

Historically,
the  invertebrate cardiovascular system has been viewed as one that is “open,”
sluggish, and poorly regulated, where blood bathes the tissues directly as it
moves through a system of sinuses and/or lacunae without an endothelial boundary.
In light of current findings, our view of the
invertebrate circulatory system and with particular emphasis on the more
complex invertebrate systems must change. The intent of this article is to draw
parallels between the more complex invertebrate circulatory architectures and
vertebrate systems using a limited and selective review of the literature to
emphasize structural and physiological complexities. We provide support for
arguments leading to a rethinking of the complexity of invertebrate circulatory
systems as well as new definitions for terms commonly used to describe various
circulatory architectures.When
cardiovascular/circulatory morphology and physiology are examined in a broad
evolutionary context, the very nature of a “closed” versus “open” circulatory
system can be questioned. Viewed in this context a number of invertebrates have
evolved incomplete or even completely cell-lined vessels and or lacunae with a
highly branched vasculature that allows for the production of significant driving
pressures and flows to meet relatively high metabolic demands driven by active
life styles. These invertebrate cardiovascular systems have well-developed
muscular pumps with complex regulatory mechanisms that facilitate a dynamic
range of responses to changing metabolic and environmental demands, and thus
have allowed the exploitation of both aquatic and terrestrial ecosystems. In fact,
many parallels can be drawn between the well-developed cardiovascular systems
of lower vertebrates to those of decapod crustacea and cephalopod Molluscs. In
light of our greater understanding of invertebrate cardiovascular systems and
their paralleled complexity to vertebrate systems, a number of long established
paradigms must be questioned and new definitions presented to better align our
understanding of the nature of “open” versus “closed” cardiovascular systems.


## 2. Why the Classic Definition of “Open” and “Closed” Circulatory Systems Must Be Rethought?

The classic view of an
open circulatory system is based on the image of pseudocoelomic or coelomic
fluid bathing the tissues directly; this fluid is circulated throughout the
coelom via the actions of the body wall musculature and animal movements. A second and somewhat more robust image of an
open system is that of a dorsally located muscular vessel or heart sitting
within a hemocoel, pumping hemolymph through anterior and/or posterior aortic
vessels. These vessels end abruptly where their contents move into the coelom
or other large space where gas, nutrient, and waste exchange take place
directly between the cells (tissues) and hemolymph (or lymph—at this point the
fluid could be described as extracellular fluid). Hemolymph then moves through venous sinuses
or simply through the coelom and into a pericardial sinus, through cardiac
ostia and into the heart for recirculation. Indeed both of these views are
technically correct, yet convey the idea of a primitive, poorly designed and
regulated cardiovascular system that is unable to sustain higher metabolic
demands (Figure1(a)).Schematics of:
(a) a classically defined “open” circulatory system (as seen in may lower
invertebrates), (b) a circulatory system that is highly complex with
capillary like vessels, a partially lined vasculature yet contains vascular
sinuses which classically has been defined as “open” yet should be categorized
as an “incompletely closed” circulatory system. (c) A classically defined
“closed” circulatory system (as seen in mammals and other higher vertebrates) ((c)
adapted from Whithers [1]). (Solid
lines represent defined vessels or a muscular pump or heart. Dashed lines
represent sinus based systems and/or vessels lacking a defined lining. Arrows
represent general patterns of blood flow. Background color is a general
indicator of arterial versus venous hemolymph or blood).
(a)(b)(c)Looking at the issue from
the other side, our standard view of a closed circulatory system is based on a
system where a multichambered muscular heart pumps blood through parallel
systemic and pulmonary circuits simultaneously (Figure1(c)). Blood is pumped
into major elastic arteries (the aorta and large arteries), which then flows
into medium and small smooth muscle-based vessels and then into arterioles,
which supply the capillary circulation.
At the capillary level, gas, nutrient, and waste exchange take place
between blood and tissues across an endothelial layer. Venous blood then
returns to the heart via, venules, small and medium veins, and finally back
into the heart via the vena cava. In the closed circulatory system at no point
does the blood leave the confines of the vascular endothelia and as such there
is a clear distinction between blood and lymph [1–3].While the descriptions
above do represent accurate depictions of the circulatory systems of worm-like
invertebrates and mammals, respectively, they do not provide the necessary
depth and breadth of information required to understand the subtle yet
significant “shades of grey” of the continuum from the invertebrate “open” and
vertebrate “closed” circulatory architecture (Figure1(b)). An exhaustive
phylogenetic review of cardiovascular morphologies is not necessary to make
this point clear. A few well-described
examples from specific taxa can be used to illustrate the complexity of the issue
and dramatically point out the shortcomings of the existing definitions.


## 3. The Typical Invertebrate “Open” Circulatory System: The Annelid Blood-Vascular System

Members
of the phyla Annelida contain some of the most complex examples of worm-like
invertebrates [5–7]. The segmented annelids have
evolved several mechanisms in order to enhance convective transport between
internal compartments. The most primitive of these being the development of a
coelom and coelomic circulation followed by the development of intracellular
iron-based oxygen binding pigments (hemoglobins), and the most advanced being a
fairly well-developed blood-vascular system [8, 9].In the
smaller annelids there are few cardio-respiratory adaptations, however; in the
larger and/or more active worms, such as the polycheates, a complex vasculature
has evolved and in the more active giant Australian earthworm (Oligocheata) a defined
heart augments the movement of blood through a well-developed vasculature (Figure
2) [10].The annelid
circulatory system, though a low pressure system, contains contractile vessels
for pumps and a highly branched vascular system. It lacks an endothelial
lining. (a) Longitudinal section, (b) cross-section of the earthworm (Lumbricus)
(adapted from R. C. Brusca and G. J. Brusca, [4]).
(a)(b)While there are many anatomical
variations observed in the cardiovascular system of annelids that appear to
have evolved due to activity patterns, feeding behaviors and environment, some
of the most complex systems are seen in the class Polychaeta.The general pattern of circulation in
polycheate worms starts with a dorsal vessel that runs just above the digestive
tract (Figure3). Blood flows anteriorly
where the dorsal vessel anastomes with a ventral vessel either directly or by
several parallel connecting vessels. The
ventral vessel runs under the digestive tract and carries blood posteriorly.Each segment of the animal receives a pair of
parapodial blood vessels that arise from the ventral vessel.The segmental parapodial vessels supply the
parapodia, the body wall (integument), and the nephridia and give rise to
intestinal vessels that supply the gut.
Blood moves from the ventral vessel through the parapodial system and
returns to the dorsal vessel through a corresponding segmental pair of dorsal
parapodial vessels (Figure 3). When gills are present and integrated  with
the blood vascular system (as opposed to being perfused with coelomic fluid)
they contain both afferent and efferent vessels (Ruppert and Barnes 1991). Pressures are generated by peristaltic waves
of contractions through the dorsal vessels. These blood vessels and their
associated blood sinuses do not contain an endothelium but are lined by only
the basal lamina of overlying cells (Figure 3) (Brusca and Brusca 1990).Figure 3
The fine
structure of the annelid (Polycheata) circulatory system.
The center diagram shows the general anatomy
of the segmentally based vascular system.
A cross-section through the body wall of the polycheates is shown on the
left with body wall, epidermal, and coelomic vessels identified. The highly
branched parapodial vasculature is outlined on the right (adapted from [11, 12].


## 4. The Atypical Invertebrate “Closed” Circulatory System: The Cardiovascular System of the Cephalopod Mollusca

The molluscan cardiovascular system has evolved extensive vascular
networks with efficient centralized pumps (e.g., true hearts) that function in
an integrated fashion with a variety of other physiological systems. The
functional significance of these complex vessels is seen in the highly active Cephalopod
Molluscs, which show the most extensive evolution and specialization of the
cardiovascular system (Figure4). Blood
is driven at high pressures by the heart through a cell-lined (closed
circulatory system) complex circulatory system that is able to sustain
metabolic rates almost equivalent to some vertebrates [13, 14]. To sustain such high oxygen uptake rates, paired branchial hearts
have evolved to pump venous blood through the gills, after which the arterial
blood flows to the ventricle where it is pumped to the systemic circuit.
Functionally, the cephalopods have evolved a multichambered heart capable of
maintaining separation between venous and arterial blood and regulating
branchial and systemic circulations. Additionally, this group of animals has
developed the cardio-respiratory regulatory mechanisms needed to integrate
cardiovascular and ventilatory performance with metabolic demands [15].
The anatomical complexity of the cardiovascular system, along with the development
of capillary-like exchange vessels, an endothelia-like vascular lining and the
appropriate regulatory mechanisms appears to have been selected for in this
group by increased activity patterns associated with predatory behavior,
swimming, and jet propulsion [12, 13].Figure 4
A generalized
schematic of the cephalopod molluscs circulatory systems (top) and a more
anatomically correct view (bottom), showing the well-developed hearts (a
ventricle and two branchial hearts) and complex, endothelial-like lined
vascular systems (peripheral and branchial). The cephalopod vascular system is
considered “closed” with highly efficient hearts pumping blood at pressures
similar to those seen in lower vertebrates (adapted from Smith and Boyle [16], Ruppert et al. [12]).While the cardiovascular systems of these more active
cephalopods are quite robust and seem to exhibit convergent evolution with some
vertebrates, in terms of their vascular complexity, there is a great deal of discrepancy
in reports as to the nature of the endothelia-like lining of the vessels and
the degree to which tissues are perfused.
It would appear that the cephalopod vascular lining is quite permeable
and may not serve as a selective barrier as in the vertebrates, which could by
some definitions make the cephalopod vascular system more “open” than “closed”
[14, 17–19]. Yet based on a more functional or physiological
definition, cephalopods exhibit a “closed” vascular system.This leads to the question: why have cephalopods
evolved both complete and/or incomplete endothelial-like lined vascular
systems?It can be hypothesized that the
invertebrate vascular lining has evolved for reasons more to do with
hemodynamics and maintaining laminar flow, than the array of functions ascribed
to the vertebrate vascular endothelia.
The evolutionary origin of the invertebrate vascular system and its
lining are derived from the coelom, yet few invertebrate taxa exhibit a
vascular endothelium [20]. Those that do are more active with
higher metabolic demands and also have well-developed centralized pumps, an
extensively branched vasculature with “capillary-like” vessels and relatively
high blood pressures.Laminar flow is required to minimize the energy needed
to move blood through these complex vascular systems. Laminar flow through a
cylindrical tube can be predicted based on vessel diameter, mean blood
velocity, and blood density and viscosity (Reynold’s number). However, if there
are sudden variations in vessel diameter or irregularities in the vessels walls
turbulent flow can result. In turbulent
flow a significantly greater pressure is required to move a fluid through the
vessels as compared to laminar flow. This is best exemplified by the fact that
in turbulent flow the pressure drop is approximately proportional to the square
of the flow rate as opposed to laminar flow where the pressure drop is
proportional to the first power of the flow rate [21, 22].It would require a robust heart and would be
energetically inefficient to move blood in a turbulent pattern through a
vasculature that changes shape abruptly and where the interiors of the vessels
are not smooth as is seen in many lacunar systems. Thus to minimize the energy required to move
blood through the cephalopod circulatory system it would be advantageous to
evolve mechanisms to facilitate laminar flow and one of which could be the
development of an endothelia-like lining [23].


## 5. New Definitions and New Views of Old Circulatory Systems

Our
current view of circulatory system architectures fits into one of two
catergories; an “open” system or a “closed” system. While there is relatively little variation
within closed systems, the same cannot be said of open systems, which appear to
vary greatly in complexity from a simple globular pump with no specialized
vessels to a more-or-less complete circulatory system. Despite the presence of
these “complete” open systems that appear to rival the complexity (both
morphologically and physiologically) (Figure1(b)) of the closed systems of
lower vertebrates, several factors continue to define them as simply “open”.A
major factor that defines a closed circulatory system as distinct from a
“complete” open system is the presence of a proper endothelium lining the
vessel walls. The circulatory systems of
all vertebrates are completely lined by an endothelial cell layer as opposed to
the invertebrates, cephalochordates, and tunicates. The vertebrate endothelium is defined as
being a continuous sheet of mesodermally derived cells lining the vasculature
(and in a broader context even more widely distributed throughout the body) are
highly active with multiple functions and are heterogeneous in structure and
function [24].
Functionally and most simply, the endothelium serves as a selective
barrier separating the blood from the tissues (i.e., defining the three
compartment system—blood,
extracellular fluid [lymph], and intracellular fluid). A more modern and
comprehensive view of endothelial function would include significant roles in
hemodynamics, hemostasis, vasomotor tone, growth, and proliferation of other
cells, antigen presentation, and metabolism of tissue or blood derived hormones
[25]. For the purposes of this discussion, a functional
barrier separating circulating blood from the tissues defines a closed
circulatory system and as such can be considered the primary function of the
endothelia or the cell-lined vasculature.Unlike
closed systems where blood and lymph are functionally separated by the
endothelium, in truly open systems these two fluids are considered to mix
freely and are thus termed hemolymph (blood and lymph). However, the presence
or absence of hemolymph does not explicitly define a system as open or closed
as comparative physiologists also define hemolymph based on the absence of
defined cell lineages (red cells, thrombocytes, and leukocytes). Thus, one may
have a cell-lined circulatory system that meets the definition of being closed
yet contains hemolymph as seen to varying degrees in the cephalopods and
crustaceans [4].The definition of open versus closed
is therefore based upon histological (endothelium) and cellular (hemolymph)
terms rather than in physiological terms (functional). How can these two
disparate views be reconciled given our new insights into the complexity of
some “open” systems? If one also considers
the circulatory system in physiological terms (which is its main function) then
this allows a rethinking of the “open” versus “closed” definition with the
addition of a new category—defined as an
“incomplete closed system” as seen in the decapod crustaceans.


## 6. An Example of the “Incomplete” Closed Circulatory System: The Decapod Crustacean

Although there are more
species of insects than any other group in the world and more individual
nematodes, crustaceans exhibit a greater variation in form and diversity than
any other animal phylum [28]. The decapod crustaceans have colonized
a wide range of environments from the deep sea through the intertidal zone, and
onto land. During the evolution of the invertebrates a number of key
adaptations were responsible for their radiation. In crustaceans, the evolution
of a segmental arterial system was a singular event that made the unique
adaptive radiation of this group possible and the evolutionary innovation that
allowed members of this group to become large and highly mobile [29].Historically, the
crustacean circulatory system has been considered open. However, during the past two decades our
knowledge of the decapod crustacean circulatory system has increased
substantially [26, 27, 29–32].The muscular ventricle is housed inside a
primer chamber, the pericardial sinus.
Heart rate and stroke volume can be controlled independently via nervous
input from the cardiac ganglion and CNS or by direct actions of neurohormones
on the cardiac muscle [29, 32]. This allows rapid
modulation of cardiac output resulting in blood pressures that rival those of
some fish and amphibians [33, 34]. Extrinsic control of cardiac function in
vertebrate systems is primarily autonomic (sympathetic excitation and
parasympathetic inhibition) layered upon intrinsic regulatory mechanisms. At
the extrinsic level of control, parallel regulatory systems are seen in the
neurogenic hearts of decapod crustaceans. Cardioacceleratory and
cardioinhibitory nerves provide input to the cardiac ganglion, modulating the
rate and force of myocardial contractions.
Additionally, the pericardial organ, an endocrine organ located on the
inner wall of the myocardium, releases a variety of neurohormones that can
modulate heart rate and cardiac contractility [32].Regional
blood flow is regulated in closed vertebrate systems by
the contraction or relaxation of vascular smooth muscle. Decapod crustaceans do
not possess smooth muscle in the artery walls [35]; instead contraction or relaxation of a pair of
muscular cardioarterial valves at the base of each arterial system
[36] controls hemolymph flow through the arteries [37, 38].A variety neurohormones have been
shown to control regional hemolymph flow (see McGaw and McMahon [39], Wilkens [29], McGaw and Reiber [26]) either by direct actions on the cardioarterial
valves or by altering downstream resistance of vessels [40, 41].
Such ability to modulate cardiac function and regional blood flow rivals
that of vertebrate systems [42, 43].In-line with
physiological control mechanisms, the anatomy of the system is equally complex.
Five arterial systems (seven individual vessels) originate from the heart, each
splitting into smaller arteries and finally into capillary-like vessels that
ramify within the tissues. Some of these vessels are similar in size
(diameter-wise) to those of vertebrate capillaries and form a true closed loop
within the brain [44, 45] and antennal gland [27] (Figure 5).
Nevertheless, decapod crustaceans lack a complete venous system; instead the
hemolymph collects in sinuses before flowing into large veins and back to the
heart. In part, it is the presence of
these sinuses that has defined the system as open. The sinuses were once
considered to be “ill-defined spaces that almost defied successful
demonstration” [46].
However, recent evidence has shown them to be more complex than
previously described, forming a network of lacunae with a morphology similar to
capillaries [27, 47], the only difference
being the lack of a true endothelial lining. One hundred and fifty years ago Haeckel [48] proposed that no unbounded lacunae exist in the crustacean
system. Major sinuses are bordered by fibrous connective tissue and the lacunae
by basal lamina directly on the organ which they bathe [49]. The
distinction between lacunae and capillary then becomes less distinct, suggesting
a more organized structure. Thus, the definition of the open system of
decapod crustaceans is really a histological term
rather than a functional one. This then
lends itself to an additional definition that would classify some of the highly
complex open systems (in both decapod crustaceans but also others such as the
cephalopods) as ones that are “incompletely closed” rather than open.Figure 5
The cardiovascular system of decapod crustaceans is highly
developed with a globular heart capable of delivering hemolymph at relatively
high pressures and flows into capillary-like vessels supplying metabolically
active tissues. This distribution system is dramatically illustrated (a) in
a corrosion cast of the blue crab’s circulatory system. The complexity of the decapod crustacean
vasculature is seen in a corrosion cast of the antennal gland ((b) from McGaw
and Reiber [26]) and a highly magnified image of the capillary like vessels
serving this structure (d) (CCA—coelomosac
artery) [27]. A transmission electron micrograph of
a cross-section through the gills also clearly shows well-defined hemolymph
channels that maximize branchial exchange ((c) from McGaw and Reiber [26]) (CH—chitinous exchange surface of lamellae; HC—hemolymph
channels; PC—pillar cells).The decapod crustacean
system exemplifies this and given the wide array of open systems the term
“incompletely closed” would describe a complex system, with a muscular heart
generating relatively high pressures, which delivers fluid through a complex
series of vessels. This will clarify some of the confusion associated with the
highly complex open systems with a complete series of vessels, versus those
that are simple and sluggish with few associated vessels or control mechanisms.



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