Comparative analysis of the circulatory system in Amphipoda (Malacostraca, Crustacea)

We present data on the haemolymph vascular system (HVS) in four representatives of the major amphipod lineages Gammaridea, Hyperiidea and Caprellidea based on corrosion casting and three‐dimensional reconstructions of histological semi‐thin sections. In all these species the HVS comprises a dorsal pulsatile heart, which is continued in the body axis by the anterior and posterior aortae. The heart is equipped with three pairs of incurrent ostia. The number of cardiac arteries that lead off the heart varies among species: in the studied Gammaridea four pairs occur, in Hyperia galba only the three posterior pairs of cardiac arteries occur, while in Caprella mutica cardiac arteries are absent. In all the studied species the posterior aorta leads as a simple tube into the pleon attached to the dorsal diaphragm. The anterior aorta runs from its origin in the anterior part of the second thoracic segment into the cephalothorax. Both pairs of antennae have an arterial supply off the anterior aorta. An overview of previously studied species including our present findings shows the amphipod HVS to be relatively uniform and the gammarid form is discussed as being closest to the ground pattern of Amphipoda.     

The circulatory system in Phreatoicidea: implications for the isopod ground pattern and peracarid phylogeny

The circulatory systems of four species of Phreatoicidea and two species of Oniscidea were studied on the basis of serial semi-thin sections and a corrosion cast method. A 3D computer reconstruction was used to visualize the circulatory organs in the head of the Phreatoicidea. In the Phreatoicidea, the circulatory system consists of a longitudinal dorsal heart extending from the third thoracic to the border between the fourth and fifth pleonal segments. It is equipped with two pairs of asymmetrically arranged ostia, while five pairs of lateral cardiac arteries and an unpaired anterior aorta extend from the heart. Entering the head, the aorta is accompanied by the two first lateral arteries, which supply the muscles of the mandibles. Four pairs of arteries branch off the aorta to supply both pairs of antennae, the eyes, and sinuses in the head. In addition, several minute capillaries extend from the aorta to supply the brain. The two oniscidean species were re-investigated with regard to some characters which have been controversially discussed. In these species, the heart extends from the border between the fifth and sixth thoracic segments to the fifth pleonal segment. Five pairs of lateral cardiac arteries and the unpaired anterior aorta lead off the heart. A ventral vessel was not observed. The ground pattern of the circulatory system in isopods is reconstructed with greater reliability through optimisation of its characters based on proposed phylogenetic relationships. The results do not support a phylogenetic position of the Isopoda as basal Peracarida or even basal Eumalacostraca.     

The circulatory system in Mysidacea--implications for the phylogenetic position of Lophogastrida and Mysida (Malacostraca, Crustacea)

The morphology of the circulatory organs in Mysida and Lophogastrida (traditionally combined as Mysidacea) is revisited investigating species so far unstudied. In addition to classical morphological methods, a newly developed combination of corrosion casting with micro computer tomography (MicroCT) and computer aided 3D reconstructions is used. Lophogastrida and Mysida show a highly developed arterial system. The tubular heart extends through the greater part of the thorax and is connected with the ventral vessel via an unpaired descending artery. It is suggested that a distinct ostia pattern supports the monophyly of Mysidacea. The cardiac artery system is more complex in Lophogastrida than in Mysida, consisting of up to 10 pairs of arteries that supply the viscera. In both taxa, an anterior and posterior aorta leads off the heart. In the anterior part of the cephalothorax the anterior aorta forms dilations into which muscles are internalized; these structures are called myoarterial formations. One of these myoarterial formations can also be found in all the other peracarid taxa but not in other Malacostraca.     

The crustacean heart ultrastructure and its bearing upon the position of the isopods in eumalacostracan phylogeny

The present paper discusses the use of myocardial ultrastructure, and its merits, in studies of crustacean phylogeny. It is argued that different modifications of the heart do not affect the membrane systems of the myofibers and that the membrane systems are independent of size and/or adaptation of the species. Finally, the phylogenetic implications of the membrane systems are considered. Using the myocardial membrane systems in addition to the cephalothorax (carapace), compound eyes, respiratory system and heart anatomy, a new phylogenetic arrangement of the larger eumalacostracan orders (Anaspidacea, Amphipoda, Cumacea, Decapoda, Euphausiacea, Isopoda, Mysidacea, Tanaidacea) is suggested. The isopods are regarded as a sister group to the other eumalacostracans.     

Evolutionary morphology of the circulatory system in Peracarida (Malacostraca; Crustacea)

We demonstrate that by formulating guidelines for evolutionary morphology the transparency, reproducibility, and intersubject testability of evolutionary hypotheses based on morphological data can be enhanced. The five main steps in our concept of evolutionary morphology are (i) taxon sampling, (ii) structural analysis, (iii) character conceptualization, (iv) phylogenetic analysis, and (v) evolutionary interpretation. We illustrate this concept on the example of the morphology of the circulatory organs in peracarid Malacostraca. The analysis is based on recently published accounts in which detailed structural analyses were carried out, and on the older literature. Detailed conceptualizations of 22 characters of the circulatory system are given for 28 terminals. In a further step these characters are included in a recently revised matrix, resulting in 110 characters. The resulting parsimony analysis yielded a single most parsimonious tree with a length of 309 steps. The most significant results are that Peracarida is monophyletic, Amphipoda is the sister taxon to the Mancoida sensu stricto, the relict cave‐dwelling taxa Thermosbaenacea, Spelaeogriphacea, and Mictocarididae form a monophylum and Tanaidacea is the sister group to a monophylum comprising Cumacea and Isopoda. The evolutionary analysis shows that the ground pattern features of the circulatory organs in Peracarida are a tubular heart extending through the whole thorax, a posterior aorta with lateral arteries, and a ventral vessel system. Important features within the Peracarida are the backward shift of the anterior border of the heart, the reduction of the ventral vessel system, and two patterns of cardiac arteries, one common to the amphipod and tanaidacean terminals, and one to the cumacean and isopod terminals. © The Willi Hennig Society 2009.     

The circulatory system and its spatial relations to other major organ systems in Spelaeogriphacea and Mictacea (Malacostraca, Crustacea) – a three-dimensional analysis

Spelaeogriphacea and Mictacea are enigmatic taxa within malacostracan crustaceans that play a pivotal role in peracarid phylogeny. Anatomical data on both taxa that are suitable for use in cladistic analyses are still scarce. Here, we provide for the first time detailed three-dimensional information on the major organ systems of Spelaeogriphacea and Mictacea (the circulatory system, the digestive system, and the central nervous system) using semithin sections in combination with computer aided three-dimensional reconstruction techniques. The digestive system in both Spelaeogriphus lepidops and Mictocaris halope is made up of a short oesophagus leading to a voluminous stomach chamber. Posteriorly, a pylorus is attached to the stomach chamber. An antechamber of the midgut glands is situated at the transition into the midgut, from which up to four tubular midgut glands emanate. The midgut is a straight tube running through the body terminating in a short hindgut. The central nervous system in the cephalothorax is made up of a brain and a suboesophageal ganglion. Both species show some reduction of the protocerebrum caused by the lack of eyes. The circulatory system is made up of a tubular heart that is situated in the thorax. It is equipped with two pairs of incurrent ostia in S. lepidops and one pair in M. halope . The only artery leading off the heart is the anterior aorta, which runs into the cephalothorax. A dilation is formed between the brain and the anterior stomach wall, into which oesophageal dilator muscles are internalized. The function of this so-called 'myoarterial formation a' as an accessory pulsatile structure in the anterior cephalothorax of these animals is discussed.  © 2007 The Linnean Society of London, Zoological Journal of the Linnean Society , 2007, 149 , 629–642.     

Peptidergic control of the heart of the stick insect, Baculum extradentatum

The dorsal vessel of the Vietnamese stick insect, Baculum extradentatum, consists of a tubular heart and an aorta that extends anteriorly into the head. Alary muscles, associated with the heart, are anchored to the body wall with attachments to the dorsal diaphragm. Alary muscle contraction draws haemolymph into the heart through incurrent ostia. Excurrent ostia lie on the dorsal vessel in the last thoracic and in each of the first two abdominal segments. Muscle fibers are associated with these excurrent ostia. Crustacean cardioactive peptide (CCAP)- and proctolin-like immunoreactivity is present in axons of the segmental nerves that project to the dorsal vessel, and in processes extending over the heart and alary muscles. Proctolin-like immunoreactive processes are also localized to the valves of the incurrent ostia and to the excurrent ostia. Neither the link nerve neurons, nor the lateral cardiac neurons, stain positively for these peptides. Physiological assays reveal dose-dependent increases in heart beat frequency in response to CCAP and proctolin. Isolating the dorsal vessel from the ventral nerve cord led to a change in the pattern of heart contractions, from a tonic, stable heart beat, to one which was phasic. The tonic nature was restored by the application of CCAP.     

Scanning electron microscopy of the dorsal vessel of Panstrongylus megistus (Burmeister, 1835) (Hemiptera: Reduviidae).

In this study we analyzed the microanatomy of the dorsal vessel of the triatomine Panstrongylus megistus. The organ is a tubule anatomically divided into an anterior aorta and a posterior heart, connected to the body wall through 8 pairs of alary muscles. The heart is divided in 3 chambers by means of 2 pairs of cardiac valves. A pair of ostia can be observed in the lateral wall of each chamber. A bundle of nerve fibers was found outside the organ, running dorsally along its major axis. A group of longitudinal muscular fibers was found in the ventral portion of the vessel. The vessel was found to be lined both internally and externally by pericardial cells covered by a thin laminar membrane. Inside the vessel the pericardial cells were disposed in layers and on the outside they formed clusters or rows.     

A change of heart: cardiovascular development in the shrimp Metapenaeus ensis

The larval development of penaeid shrimp is among the most complicated in crustaceans. In Metapenaeus ensis, there are six naupliar, three protozoeal and three mysid larval instars, followed by postlarval development. Irregular heartbeat begins late in naupliar instar 6. Co-ordinated beating at 400-600 beats min(-1) commences in the first protozoeal instar and continues throughout larval life. Initially, the contractile region is located more posteriorly in the cephalothorax and has a single pair of ostia, and the arterial distribution is limited to a single anterior vessel. In later mysid instars, a second cardiac pumping site develops posterior to, but connected with, the original site. This extension is more muscular, contains additional ostia and develops additional distribution vessels supplying the cephalothorax and abdominal areas. The original site is gradually merged into the new extension and only small refinements in the circulation occur in postlarval and juvenile life. Changes in physiological responses of the heart also occur throughout development. Responses to intra-pericardial microinjection of 5-hydroxytryptamine change drastically during development, as do cardiac responses to ambient hypoxia. Similarly, heartbeat of later juvenile instars is inhibited by injection of tetrodotoxin, while heartbeat of larval and early juvenile instars is not, suggesting that neurogenic regulation via the cardiac ganglion arises later in development. Our present studies attempt to integrate the anatomical and physiological changes in the development of the crustacean heart.     

Ventilatory and cardiovascular modulation associated with burying behaviour in two sympatric crab species, Cancer magister and Cancer productus

Physiological parameters associated with burying were investigated in the Dungeness crab, Cancer magister, and the red rock crab, Cancer productus. Ventilation frequency of the branchial chambers increased while the crabs were burying, this was associated with the greater oxygen demand of the tissues. The number of ventilatory reversals in C. magister increased in number as well as in duration and magnitude when the crabs were buried, which functioned to clear the branchial chambers of sediment. In contrast, the number of ventilatory reversals in C. productus decreased. On the surface of the sand, cardiac parameters (heart rate, stroke volume, cardiac output) of both species remained stable. During the burial process, there was a large increase in cardiac output which was afforded primarily by an increased stroke volume of the heart. Once buried, cardiac output declined in both species; this was due to a decrease in stroke volume in C. productus, but a decreased heart rate in C. magister. There were also differences in haemolymph flows through each arterial system. During the burying process, both species increased haemolymph flow to the muscles of the limbs via the sternal artery. Once buried haemolymph flows to the limbs decreased, and increased flow to eyestalks and antennae via the anterior aorta occurred. Perfusion of the digestive organs via the anterolateral and hepatic arteries did not change when the crabs were buried. There was an increase in flow through the posterior aorta, of C. magister, but flow through this artery did not change in C. productus. Periods of spontaneous cardiac arrest were observed in both species while resting on the surface. These increased in duration in C. productus when buried, but there was no change in C. magister. Changes in ventilatory and cardiac variables were closely linked on the surface, but tended to uncouple when the animals were buried. The physiological responses of C. magister resembled those of true sand-dwelling crabs, whereas the responses of C. productus paralleled those of crabs that only bury occasionally in the substrate. Although these two species often occur sympatrically, they employ different physiological mechanisms when buried in the sediment.     

Functional morphology of the dorsal vessel in the adult fly Protophormia terraenovae (diptera,calliphoridae)

The morphology and ultrastructure of the contractile tubular vessel acting as the cardiac pump in Protophormia terraenovae flies were analyzed by means of light microscopy, SEM and TEM. The results provide a novel anatomical picture of the two vessel portions, the abdominal heart and the aorta, and lay the foundations for an interpretation of the cardiocirculatory function in the fly. In the thorax, the thin and unchambered aorta is without apertures, while the abdominal heart presents a very small caudal aperture and pairs of lateral ostia, one in each of the five chambers of which it is composed. The ostia of the four more distal chambers are of the incurrent type, which is to say that they act as valves ensuring that hemolymph flows only into the heart. Conversely, the ostia in the most proximal chamber allow hemolymph to flow both into and out of the heart. The entire vessel is composed of a single layer of myofibers that are oriented circularly around the lumen in the abdominal heart and longitudinally in the thoracic aorta. The abdominal heart has a thicker wall, a far more diffused and thick distribution of tracheoles, and a far greater number of mitochondria with respect to the aorta. This arrangement ensures a greater availability of oxygen and energy in the abdominal heart compared to the aorta and leads one to suppose that the high‐ and low‐frequency contractions of the cardiac cycle (Thon, [1982] J. Insect Physiol. 28:411–416) can be attributed to the abdominal heart and the aorta, respectively. J. Morphol. 240:15–31, 1999. © 1999 Wiley‐Liss, Inc.     

Comparative morphology of the hemolymph vascular system in scorpions--a survey using corrosion casting, MicroCT, and 3D-reconstruction

Although scorpions are one of the better known groups of Arthropoda, detailed knowledge of their anatomy remains superficial. This contribution presents the first comprehensive investigation of the gross morphology of the scorpion vascular system, based on a survey of species representing all major lineages of the order, using classical and modern non-destructive techniques in combination with three-dimensional reconstruction. The investigation reveals that the hemolymph vascular system (HVS) of Scorpiones comprises a central pumping heart which extends the entire length of the mesosoma and is enclosed in a pericardium. Several arteries branch off the heart to supply different organs and body regions. Two different anterior aorta major branching patterns are identified among the species investigated. Arteries that branch off the anterior aorta system supply the appendages (chelicerae, pedipalps, and walking legs) and the central nerve mass with a complex arterial network. This study of the HVS of scorpions provides further evidence that the vascular systems of euarthropods can be highly complex. Use of the term "open circulatory system" within arthropods is re-emphasized, as it refers to the general organization of the body cavity (i.e. mixocoely) rather than to the complexity of the circulatory system.     

Functional morphology of the heart and of a new cephalic pulsatile organ in the blowfly Calliphora vicina (Diptera: Calliphoridae) and their roles in hemolymph transport and tracheal ventilation

In the blowfly Calliphora vicina (Diptera: Calliphoridae), the morphology of the dorsal vessel and of a new cephalic accessory pulsatile organ (CPO) were analysed with light-microscopic, SEM and TEM techniques. The CPO and neck aorta are reconstructed 3-dimensionally by computer-aided design. The pulse activity of the CPO and of the heart was measured in intact flies over periods of several hours or days using contact-thermography with laser beam heat-marking. The intratracheal pressure was simultaneously measured at the anterior thoracic spiracle. The dorsal vessel is constructed of pairs of left–right alternating cells. Its enlarged chamber in the anterior abdomen contains two pairs of incurrent ostia, its posterior narrower heart tube possesses three pairs of incurrent ostia and paired caudal excurrent openings. The aorta opens with a funnel-like opening in the neck. Proportions, arrangement and ultrastructure of the aorta, heart cells and pericardial muscles are described. Cushionlike sarcoplasmic protrusions of heart cells (pair no. 17) probably function as internal valves. The neck aorta is constructed of a cuticular ‘roof’ deviating from the dorsal neck membrane and a ventral longitudinal muscle ‘floor’. The aorta is not kept open because of missing muscle or connective tissue strands. The underside of the CPO is fused with air sacs that function as antagonists to the muscles. The heart reverses its beat periodically in resting and active flies. During the longer forward-pulse periods, mean frequency is lower (about 3.0 Hz at Ta 20°C), during the shorter backward periods mean frequency is higher (4.6 Hz). The CPO beats only during forward-pulse periods of the heart with an independent and slower pulse rate (1.8 Hz). The CPO-pulses produce positive pressure pulses at the anterior thoracic spiracle. During backward-pulse periods of the heart and pulse pause of the CPO, a continuous negative pressure arises at the thoracic spiracle instead of pressure pulses. The intimate connection of an accessory pulsatile organ with tracheal air sacs makes it work as a bifunctional pump for hemolymph distribution and tracheal ventilation. Neurosecretory and synapsing innervation of the CPO in connection with aorta, heart and pericardial septum muscle innervation suggest that both organs are regulated and that the duration of their periods is neuronally coordinated.     

Females of the marine amphipod Jassa marmorata mate multiple times with the same or different males

Cardiovascular and respiratory variables were recorded in the blue crab, Callinectes sapidus, during injury and subsequent autotomy of a chela. Cardiac function and haemolymph flow rates were measured using a pulsed-Doppler flowmeter. Oxygen uptake was recorded using an intermittent flow respirometry system. Crabs reacted to the loss of a chela with a rapid increase in heart rate, which was sustained for 2?h. Stroke volume of the heart also increased after the chela was autotomized. A combined increase in heart rate and stroke volume led to an increase in cardiac output, which was maintained for an hour after the loss of a chela. There was also differential haemolymph perfusion of various structures. There was no change in perfusion of the anterolateral arteries or posterior and anterior aortae, during injury of the chela or subsequent autotomy. Haemolymph flow rates did increase significantly through the sternal artery during injury and immediately following autotomy of the chela. This was at the expense of blood flow to the digestive gland: a sustained decrease in haemolymph flow through the hepatic arteries occurred for 3?h following autotomy. Fine-scale cardiac changes associated with the act of autotomy included a bradycardia and/or associated cardiac pausing before the chela was shed, followed by a subsequent increase in cardiac parameters. Changes in the cardiovascular physiology were paralleled by an increase in oxygen uptake, which was driven by an increased ventilation of the branchial chambers. Although limb loss is a major event, it appears that only acute changes in physiology occur. These may benefit the individual, allowing rapid escape following autotomy with a subsequent return to normal activity.     

Morphology of the dorsal vessel in the abdomen of the blood-feeding insect Rhodnius prolixus

The dorsal vessel (DV) in the abdomen of the blood-feeding insect Rhodnius prolixus was divided functionally into two regions, the heart, into which haemolymph entered the DV through four pairs of ostia located in abdominal segment VII, and the aorta, along which the haemolymph was propelled from abdominal segment VI to the thorax. Osmium-fixed whole mounts revealed the DV to consist of spirally arranged striated muscle fibers and to possess two rows of ventrally attached longitudinal fibers extending the length of the abdomen. Seven pairs of alary muscles were found attached to the DV in the posterior abdominal segments. Contractions of the alary muscles attached to the ventral surface of abdominal segments VII and VIII served to expand the heart. Electron microscopy revealed the DV to consist of a thin layer of contractile elements surrounded by an inner (intima) and outer (adventitia) connective tissue layer. Embedded in the intima along each lateral side of the DV were two large groups of endocardial cells extending the length of the DV. A small group of pericardial cells was embedded in the adventitia along the mid-ventral side of the DV, and clusters of pericardial cells were found attached to the alary muscles. Nerve terminals were found only on the heart: they contained agranular synaptic vesicles approximately 30 nm in diameter and densely stained granules approximately 100-120 nm in diameter. These structural components are discussed in relation to the role of the DV in circulation.     

Cardiovascular and respiratory responses associated with limb autotomy in the blue crab, Callinectes sapidus

Cardiovascular and respiratory variables were recorded in the blue crab, Callinectes sapidus, during injury and subsequent autotomy of a chela. Cardiac function and haemolymph flow rates were measured using a pulsed-Doppler flowmeter. Oxygen uptake was recorded using an intermittent flow respirometry system. Crabs reacted to the loss of a chela with a rapid increase in heart rate, which was sustained for 2 h. Stroke volume of the heart also increased after the chela was autotomized. A combined increase in heart rate and stroke volume led to an increase in cardiac output, which was maintained for an hour after the loss of a chela. There was also differential haemolymph perfusion of various structures. There was no change in perfusion of the anterolateral arteries or posterior and anterior aortae, during injury of the chela or subsequent autotomy. Haemolymph flow rates did increase significantly through the sternal artery during injury and immediately following autotomy of the chela. This was at the expense of blood flow to the digestive gland: a sustained decrease in haemolymph flow through the hepatic arteries occurred for 3 h following autotomy. Fine-scale cardiac changes associated with the act of autotomy included a bradycardia and/or associated cardiac pausing before the chela was shed, followed by a subsequent increase in cardiac parameters. Changes in the cardiovascular physiology were paralleled by an increase in oxygen uptake, which was driven by an increased ventilation of the branchial chambers. Although limb loss is a major event, it appears that only acute changes in physiology occur. These may benefit the individual, allowing rapid escape following autotomy with a subsequent return to normal activity.