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«Obenchain, F. D., and J. H. Oliver, Jr. 1976. The heart and arterial circulatory system of ticks (Atari : (Ixodioidea). J. Arachnol. 3 ...»

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Obenchain, F. D., and J. H. Oliver, Jr. 1976. The heart and arterial circulatory system of ticks (Atari :

(Ixodioidea). J. Arachnol. 3 :57-74.

THE HEART AND ARTERIAL CIRCULATORY SYSTEM

OF TICKS (ACARI : IXODOIDEA) '

Frederick D. Obenchai n

James H. Oliver, Jr.

Institute of Arthropodology and Parasitology

Department of Biology, Georgia Southern Colleg e

Statesboro, Georgia 3045 8

ABSTRAC T The heart and arterial (efferent) circulatory system in Argas radiatus and Ornithodoros turicata (Argasidae) and in Ixodes scapularis, Dermacentor variabilis and Amblyomma tuberculatum (Ixodidae ) are consistent in form with the plan observed in other apulmonate Arachnida. Specialized sinuses or vessels for channelization of venous (afferent) hemolymph are absent, but heart, arterial vessels an d sinuses are well-developed. The heart lies in a sinus formed by the pericardial septum which i s continuous with connective tissue processes of dorso-lateral and ventro-lateral suspensory muscles o f the heart. Hemolymph flows from the pericardial sinus into two segmental cardiac cavities via tw o pairs of ostia. Walls of this pulsatile portion of the heart are formed from radiating muscle bands. On contraction, hemolymph is pumped through an anterior thin-walled heart region (aortic-myocardia l cone), past an aortic septal valve which prevents back flow, into the anterior aortal and on to th e periganglionic sinus. Hemolymph reaches peripheral parts of the body via arterial vessels whic h surround the pedal nerve trunks. Hemolymph also flows anteriorly, through the periesophageal sinu s which surrounds the esophagus and the pharyngeal musculature, and into vessels surrounding nerves t o the capitular appendages.

An endosternum is present in argasid ticks. Its reported continuity with tissues forming the periganglionic sinus walls is confirmed in this group. No trace of an endosternum is observed in ixodi d ticks. Loss of the endosternum appears to facilitate the extensive engorgement behavior observed in ixodid females. Extrinsic muscles present in the periganglionic sinus of all investigated tick specie s may be derived from dorso-ventral suspensory muscles of a prototypic endosternum. These muscles, together with the intrinsic muscles in the ventral wall of the aorta and the action of the aortic septa l valve, may function in the maintenance of elevated arterial pressures. The specialized structure of the ventro-lateral suspensory muscles of the heart suggests that they may play an important role a s proprioceptors. The presence of a highly condensed and regionally specialized heart, the existence of a pericardial sinus, and specializations of arterial vessels and sinuses, attest to the complexity an d evolutionary advancement of the circulatory system in Ixodoid.ea.

INTRODUCTION

Classical data on the form of the heart and arterial circulatory system in ticks com e from general anatomical studies by Christophers (1906) on species of Ornithodoros and Hyalomma, Nordenskiold (1909) on Ixodes, Robinson and Davidson (1913-1914) o n Argas, and Douglas (1943) on Dermacentor. Although there are many contradictor y ' Supported by Public Health Service Research Grant AI-09556 from the National Institute of Allerg y and Infectious Diseases (Principal Investigator, J. H. Oliver, Jr.).

–  –  –

details in these reports, they indicate the presence of characteristic features from th e basic plan of apulmonate arachnid-type circulatory systems in representative Argasida e and Ixodidae.

In Arthropoda the open-type circulatory system is considered an evolutionary con sequence of the disintegration of coelomic walls which were present in their ancestra l annelid-like prototypes (Beklemishev, 1968). Most arthropods retain only the dorsal pulsatile vessel (heart) and a few associated lateral arches of the annelid closed-typ e system. Certain higher Crustacea, some Myriapoda, larval Xiphosura and most pulmonat e Arachnida (those taxa with book lungs) also retain ventral vessels (the paired thoraci c arterial sinuses of Firstman, 1973) in association with the ganglionic chain of the centra l nervous system. Together, these vessels function as an arterial system ; hemolymph is pumped through their branches into lacunar spaces in the body and appendages.

In those Xiphosura and pulmonate Arachnida (including the Scorpiones, Uropygi, Amblypygi and Araneae) which have been investigated (Kaestner, 1968 ; Firstman, 1973 ) hemolymph passes ventrally from lacunae of the appendages and body into one or mor e venous sinuses. Within connective tissue-lined extensions of these cavities it is channele d through the gills or leaves of the book lungs where dissolved respiratory pigments (hemocyanins) are oxygenated. Several pairs of lateral dorso-ventral sinuses, incorrectly calle d veins, transport oxygenated hemolymph to the pericardial cavity, a specialized sinu s surrounding the multi-segmented heart and other portions of the dorsal vessel. The hear t is suspended within the pericardial sinus by a series of dorso-lateral and ventro-latera l muscles or elastic ligaments (Stewart and Martin, 1974). During diastole the recoil o f these tissues expands the previously contracted heart and hemolymph is pumped forwar d through the anterior aorta. Simultaneously, hemolymph may be pumped laterally through segmentally arranged lateral arteries or to the rear through a posterior aorta.





Anatomical data on the circulatory system in apulmonate Arachnida (including th e Palpigradi, Opiliones, Acari, Pseudoscorpiones, Ricinulei and Solifugae) are limited (First man, 1973). Nevertheless, consistent differences between the pulmonate and apulmonate-type plans are known. In apulmonate arachnids, particularly those which show reductions in number of body tagmata, the heart is more condensed and the anterio r (dorsal) aorta more highly differentiated, but unbranched (Beklemishev, 1969). In place of ventral vessels the thoracic arterial sinuses are expanded as a perineural sinus enclosing the entire central nervous system (Kaestner, 1968 ; Firstman, 1973). This perineural sinu s receives the aorta and gives rise to an anterior (periesophageal) sinus and lateral arteria l vessels which surround nerve trunks to the appendages. Hemolymph passes from thes e vessels into lacunae within each appendage, then flows into the general body lacunae and, finally, back to the heart.

Although preliminary anatomical studies have been made on the heart and arteria l circulatory systems of ticks and other apulmonate Arachnida, there is no firm anatomica l basis for the investigation of physiological and pharmacological processes. Such studie s have not been initiated despite the relative ecological and economic importance of thes e taxa. The small size of most parasitic Acari makes them unsuitable for many basi c anatomical and physiological investigations, but the larger size of ticks (Ixodoidea) an d their importance as vectors of disease (Balashov, 1972) make them prime subjects fo r such studies. Furthermore, the possibly critical role of the circulatory system durin g feeding in Ixodidae makes an understanding of this system particularly important. Our previous examination of the central nervous system (Obenchain, 1974a) and neurosecretory system of Dermacentor variabilis (Obenchain, 1974b ; Obenchain and Oliver,

OBENCHAIN AND OLIVER—CIRCULATORY SYSTEM OF TICKS 59

1975) revealed the probable involvement of tissues forming the wall of the aorta an d periganglionic arterial sinus in neuroendocrine mechanisms. The present study was under taken as the basis for further studies on the roles of tick cardioglial tissues in suc h mechanisms and to provide the anatomical data prerequisite to a fuller understanding o f the functional role(s) of the circulatory system in engorged and unengorged ticks.

MATERIALS AND METHOD S

Anatomical and histological observations on tick hearts and arterial circulator y systems were made on laboratory-reared and wild-caught specimens representing fou r sub-families from the two major tick families. Species examined include Argas radiatu s Railliet (Argasidae : Argasinae), Ornithodoros turicata (Duges) (Argasidae : Ornithodorinae), Ixodes scapularis Say (Ixodidae : Ixodinae), and Dermacentor variabilis (Say) and Amblyomma tuberculatum Marx (Ixodidae : Amblyomminae). Laboratory rearing conditions, tick-hosts and collection data were reported previously (Obenchain an d Oliver, 1973). Anatomical observations on the heart of intact nymphal and adult tick s were facilitated by application of paraffin oil to the tick 's dorsum. Under these conditions the cuticle became semi-transparent. Although the transparent heart musculatur e and associated tissues could not be observed directly, heart position and its rate of contraction were determined from the movements of tracheae and tracheoles. Detaile d structural observations were made on dorsal and ventral dissections of the circulator y system, performed under Shen's physiological saline (9.0 g NaCl, 0.42 g KC1,

0.25 g CaC1 4 /liter of distilled water).

Some dissections were made on specimens previously injected with supravital dyes, including 0.5% ammoniacal carmine, 0.02-0.5% trypan blue in Shen's saline, or 1.0 % methylene blue in 1.3% NaCl. Other dissections were stained in toto with leucomethylen e blue (about 0.1% after reduction with O.O1M ascorbic acid, Larimer and Ashby, 1964) fo r demonstration of neural elements. Whole mount preparations of the circulatory syste m were fixed in a calcium formal or 5% ammonium molybdate for direct microscopi c examination. Other dissections were fixed in Heidenhain's SUSA or Carnoy's fixative s (Humason, 1967) and routinely dehydrated in Cellosolve, embedded in Tissuemat Paraplast by the dioxane method, and sectioned at 7 gm. Staining techniques included Hubschman ' s (1962) simplified azan and Rosa's aldehyde fuchsin with Halmi ' s counter stain (Meola, 1970). Fresh or vitally stained tissues were stretched on slides in Shen' s saline or 50% glycerol in distilled water for examination by bright field, dark field / fluorescence, phase contrast, or polarized light microscopy. Histological sections were dehydrated through xylene, mounted in Harleco synthetic resin and examined with the above mentioned optics. Photomicrographs were taken on a Wild M20KGS photomicroscope. Dimensions of tissues were determined with an ocular micrometer and fro m calibrated photomicrographs.

OBSERVATIONS

In all examined tick species the heart (Ht) is suspended by a series of dorso-lateral an d ventro-lateral suspensory muscles (d1SM, v1SM) within a pericardial sinus (pcS) locate d medially below the dorsal cuticle. The heart and tissues forming the boundries of the pericardial sinus are bordered anteriorly by insertions of the cheliceral retractor muscle s (Figs. 1, 2). Laterally, they lie between mid-dorsal loops of the malpighian tubules and

60 THE JOURNAL OF ARACHNOLOGY

Fig. 1.-Diagrammatic representation of the heart, pericardial septum, suspensory muscles an d associated tissues of Amblyomma tuberculatum, in ventral view. Scale equals 0.1 mm. Ao, anterior aorta ; AoMC, aortic-myocardial cone ; ChRM, cheliceral retractor muscles ; d1SM, dorso-lateral suspensory muscles ; GdT-dF, glandular tissues of the dorsal foveae ; Ht-P, pulsatile portion of the heart ;

Ost, ostia ; pdvBM, posteromedian dorso-ventral body muscles ; pcSp, pericardial septum ; vlSM, ventrolateral suspensory muscles.

insertions of the dorso-genital muscles (and by insertions of the coxal adductor muscle s III and IV in Argasidae). Posteriorly, they are bordered by insertions of the posteromedian dorso-ventral body muscles (and by tissues associated with the dorsal foveae i n Ixodidae-Amblyomminae). The tick heart is in the form of a dorso-ventrally flattene d sack. During diastole the heart outline is sub-triangular (Argasidae) to pentagonal (Ixodidae, Fig. 1), but generally spherical in the contracted state (Figs. 4, 5). The thin walled aorta (Ao) emerges from the anterior apex of the heart and runs forward belo w the cheliceral retractor muscles and above the central portion of the midgut (Fig. 2). At the median notch between the anterior ramifications (caeca) of the midgut, the aorta

–  –  –

A' Figs. 2, 3.—Diagrammatic representation of the form and anatomical associations of heart, arteria l

sinuses and vessels in a representative male ixodid tick (about the size of Dermacentor variabilis) :

2, Near-sagittal reconstruction, with addition of a cheliceral shaft, associated muscles, and dorsa l foveae (non-mid-line structures) ; 3, Cross-sections of tick arterial sinuses at levels indicated in Fig.

2. Scale on figures equals 0.1 mm. Ao, anterior aorta ; AoSV, aortic septal valve ; Cap, capitulum ;

ChRM, cheliceral retractor muscles ; ChS, cheliceral shaft ; chN, cheliceral nerves ; daS, dorsal anterior sinus ; dF, dorsal foveae ; E, esophagus ; exM, extrinsic muscles of the periganglionic sinus ; GdT-dF, glandular tissues of the dorsal foveae ; Gen Acc Gd, male genital accessory gland ; Ht, heart ; hN II, second hemal nerve ; lsN, lateral "sympathetic" nerve ; MG, midgut ; optN, optic nerves ; Ph, pharynx ;

PhM, pharyngeal musculature ; pcSp, pericardial septum ; peS, periesophageal sinus ; pgS,, periganglioni c sinus ; p II Vs, second pedal arterial vessels ; Scut, scutum ; Syn, synganglion ; stN, stomodeal nerve ;

VasM, vascular membrane ; vaS, ventral anterior sinus.

descends into the periganglionic arterial sinus (pgS). No traces of a posterior aorta ar e observed in any of the examined tick species.

Anatomically, the periganglionic sinus and associated arterial vessels of Dermacentor variabilis are representative of similar circulatory structures in other tick species. Sinu s walls completely envelop the condensed mass of the central nervous system (synganglion)

62 THE JOURNAL OF ARACHNOLOG Y



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