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The Arthropod Circulatory System

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Arthropod Biology and Evolution

Abstract

Arthropods have a genuine circulatory system. Their exoskeleton encloses a liquid-filled body cavity, the haemocoel. Thereby all organs and tissues are permanently exposed to a fluid medium, the haemolymph which consists of plasma with suspended haemocytes. The circulation of haemolymph is actively forced by special pumping organs referred to as hearts. Emanating from the hearts, arteries deliver the haemolymph to the various body regions and compartments. These arterial systems are developed to differing extents in arthropods and together with the heart constitute the cardiovascular system or haemolymph vascular system. As haemolymph leaves the vascular system, it empties into the lacunar system, where it follows distinct routes that are determined by the anatomy of the internal organs and by channels or diaphragms formed of connective tissue. This article reviews major features and functions of the arthropod circulatory system. It describes the great disparity in the anatomy of the circulatory organs among the major arthropod lineages, their development and evolution. A special focus refers to the evolutionary changes which this organ system has undergone along the major environmental transitions from aquatic to terrestrial habitats and the evolution of flight.

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References

  • Ai H, Kuwasawa K (1995) Neural pathways for cardiac reflexes triggered by external mechanical stimuli in larvae of Bombyx mori. J Insect Physiol 41:1119–1131

    CAS  Google Scholar 

  • Alexandrowicz JS (1932) The innervation of the heart of Crustacea I. Decapoda. Q J Microsc Sci 75:182–247

    Google Scholar 

  • Andereck JW, King JKG, Hillyer JF (2010) Contraction of the ventral abdomen potentiates extracardiac retrograde hemolymph propulsion in the mosquito hemocoel. PLoS ONE 5(9):e12943. doi:10.1371/journal.pone.0012943

  • Anderson DT (1973) Embryology and phylogeny in annelids and arthropods. Pergamon Press, Oxford

    Google Scholar 

  • Angioy AM, Boassa D, Dulcis D (1999) Functional morphology of the dorsal vessel in the adult fly Protophormia terraenovae (Diptera, Calliphoridae). J Morphol 240:15–31

    Google Scholar 

  • Angioy AM, Pietra P (1995) Mechanism of beat reversal in semi-intact heart preparations of the blowfly Phormia regina (Meigen). J Comp Physiol B 165:165–170

    Google Scholar 

  • Arnold JW (1964) Blood circulation in insect wings. Mem Entomol Soc Can 38:5–60

    Google Scholar 

  • Balss H, Buddenbrock Wv, Gruner HE, Korschelt E (1940–61) Decapoda. In: Schellenberg A, Gruner HE (eds) Bronn’s Klassen und Ordnungen des Tierreichs. Akademische Verlagsgesellschaft Geest and Portig, Leipzig

    Google Scholar 

  • Bartolomaeus T, Quast B, Koch M (2009) Nephridial development and body cavity formation in Artemia salina (Crustacea: Branchiopoda): no evidence for any transitory coelom. Zoomorphology 128:247–262

    Google Scholar 

  • Baumann H (1921) Das Gefäßsystem von Astacus fluviatilis (Potamobius L.). Z wiss Zool 118:246–312

    Google Scholar 

  • Baum E, Hertel W, Beutel RG (2007) Head capsule, cephalic central nervous system and head circulatory system of an aberrant orthopteran, Prosarthria teretrirostris (Caelifera, Hexapoda). Zoology 110:147–160

    PubMed  Google Scholar 

  • Belman BW, Childress JJ (1976) Circulatory adaptations to the oxygen minimum layer in the bathypelagic mysid Gnathophausia ingens. Biol Bull 150:15–37

    PubMed  CAS  Google Scholar 

  • Bier E, Bodmer R (2004) Drosophila, an emerging model for cardiac disease. Gene 342:1–11

    PubMed  CAS  Google Scholar 

  • Bodmer R, Frasch M (2010) Development and aging of the Drosophila heart. In: Rosenthal N, Harvey RP (eds) Heart development and regeneration. Academic, San Diego, pp 47–86

    Google Scholar 

  • Brigandt I, Love AC (2012) Conceptualizing evolutionary novelty: moving beyond definitional debates. J Exp Zool B Mol Dev Evol 318:417–427

    PubMed  Google Scholar 

  • Brocher F (1909) Sur l’organe pulsatile observé dans les pattes des hémiptères aquatiques. Ann Biol Lacustre 4:33–41

    Google Scholar 

  • Brodsky AK (1994) The evolution of insect flight. Oxford University Press, New York

    Google Scholar 

  • Bryantsev AL, Cripps RM (2009) Cardiac gene regulatory networks in Drosophila. Acta Biochim Biophys 1789:343–353

    CAS  Google Scholar 

  • Burnett BR (1972) Aspects of the circulatory system of Pollicipes polymerus J. B. Sowerby (Cirripedia: Thoracica). J Morphol 136:79–107

    Google Scholar 

  • Burnett BR (1984) Striated muscle in the wall of the dorsal abdominal aorta of the California spiny lobster Panulirus interruptus. J Crustac Biol 4:560–566

    Google Scholar 

  • Cannon HG (1947) On the anatomy of the pedunculate barnacle Lithotrya. Phil Trans R Soc B 595:89–136

    Google Scholar 

  • Chan KS, Cavey MJ, Wilkens JL (2006) Microscopic anatomy of the thin-walled vessels leaving the heart of the lobster Homarus americanus: anterior lateral arteries. Invertebr Biol 125:70–82

    Google Scholar 

  • Chapman RF (1998) The insects: structure and function, 4th edn. Cambridge University Press, Cambridge

    Google Scholar 

  • Clements AN (1956) The antennal pulsatile organs of mosquitoes and other Diptera. Q J Microsc Sci 97:429–435

    Google Scholar 

  • Cooke IM (2002) Reliable, responsive pacemaking and pattern generation with minimal cell numbers: the crustacean cardiac ganglion. Biol Bull 202:108–136

    PubMed  Google Scholar 

  • Cripps RM, Olson EN (2002) Control of cardiac development by an evolutionarily conserved transcriptional network. Dev Biol 246:14–28

    PubMed  CAS  Google Scholar 

  • Curtis NJ, Ringo JM, Dowse HB (1999) Morphology of the pupal heart, adult heart, and associated tissues in the fruit fly, Drosophila melanogaster. J Morphol 240:225–235

    PubMed  CAS  Google Scholar 

  • Davis N-T, Dulcis D, Hildebrand JG (2001) Innervation of the heart and aorta of Manduca sexta. J Comp Neurol 440:245–260

    PubMed  CAS  Google Scholar 

  • Debaisieux P (1936) Organes pulsatiles des tibias de Notonectes. Ann Soc Sci Brux B 56:77–87

    Google Scholar 

  • Dohle W (1985) Phylogenetic pathways in the Chilopoda. Bijdr Dierk 55:55–66

    Google Scholar 

  • Dubuisson M (1928) Recherches sur la circulation du sang chez les Crustacés. 1er note: Amphipodes. Circulation chez les Gammariens; synchronisme des mouvements respiratoires et des pulsations cardiaque. Arch Zool Exp Gen 67:93–104

    Google Scholar 

  • Dudley R (2000) The biomechanics of insect flight. Princeton University Press, Princeton

    Google Scholar 

  • Dulcis D, Davis NT, Hildebrand JG (2001) Neuronal control of heart reversal in the hawkmoth Manduca sexta. J Comp Physiol A 187:837–849

    PubMed  CAS  Google Scholar 

  • Dulcis D, Levine RB (2003) Innervation of the heart of the adult fruit fly, Drosophila melanogaster. J Comp Neurol 465:560–578

    PubMed  Google Scholar 

  • Dulcis D, Levine RB (2005) Glutamatergic innervation of the heart initiates retrograde contractions in adult Drosophila melanogaster. J Neurosci 25:271–280

    PubMed  CAS  Google Scholar 

  • Duman-Scheel M, Pirkl N, Patel NH (2002) Analysis of the expression pattern of Mysidium columbiae wingless provides evidence for conserved mesodermal and retinal patterning processes among insects and crustaceans. Dev Genes Evol 212:114–123

    PubMed  CAS  Google Scholar 

  • Dumont JN, Anderson E, Chomyn E (1965) The anatomy of the peripheral nerve and its ensheathing artery in the horseshoe crab, Xiphosura (Limulus) polyphemus. J Ultrastruct Res 13:38–64

    PubMed  CAS  Google Scholar 

  • Eberhard WG, Huber BA (1998) Courtship, copulation, and sperm transfer in Leucauge mariana (Araneae, Tetragnathidae) with implications for higher classification. J Arachnol 26:342–368

    Google Scholar 

  • Ellis CH (1944) The mechanism of extension in the legs of spiders. Biol Bull 86:41–50

    Google Scholar 

  • Fahlander K (1938) Beiträge zur Anatomie und systematischen Einteilung der Chilopoden. Zool Bidr Uppsala 17:1–148

    Google Scholar 

  • Farley RD (1985) Cardioregulation in the desert scorpion, Paruroctonus mesaensis. Comp Biochem Physiol 82C:377–387

    CAS  Google Scholar 

  • Farley RD (1987) Postsynaptic potentials and contraction pattern in the heart of the desert scorpion, Paruroctonus mesaensis. Comp Biochem Physiol 86A:121–131

    Google Scholar 

  • Farley RD (2010) Book gill development in embryos and first and second instars of the horseshoe crab Limulus polyphemus L. (Chelicerata, Xiphosura). Arthropod Struct Dev 39:369–381

    PubMed  Google Scholar 

  • Firstman B (1973) The relationship of the chelicerate arterial system to the evolution of the endosternite. J Arachnol 1:1–54

    Google Scholar 

  • Fraisl P, Mazzone M, Schmidt T, Carmeliet P (2009) Regulation of angiogenesis by oxygen and metabolism. Dev Cell 16:167–179

    PubMed  CAS  Google Scholar 

  • Frank H (1957) Untersuchungen zur funktionellen Ana-tomie der lokomotorischen Extremitäten von Zygiella x-notata, einer Radnetzspinne. Eberhard-Karls-Universität zu Tübingen, Dissertation

    Google Scholar 

  • Freudenstein K (1928) Das Herz und das Circulationssystem der Honigbiene (Apis mellifica L.). Z Wiss Zool 132:404–475

    Google Scholar 

  • Gereben-Krenn B-A, Pass G (1999) Circulatory organs of Diplura (Hexapoda): the basic design in Hexapoda? Int J Insect Morphol 28:71–79

    Google Scholar 

  • Gereben-Krenn B-A, Pass G (2000) Circulatory organs of abdominal appendages in primitive insects (Hexapoda: Archaeognatha, Zygentoma and Ephemeroptera). Acta Zool 81:285–292

    Google Scholar 

  • Gerhardt U, Kästner A (1938) Araneae. In: Kükenthal WG, Krumbach T (eds) Handbuch der Zoologie, vol 3. De Gruyter, Berlin, pp 394–656

    Google Scholar 

  • Gerould JH (1933) Orders of insects with heart-beat reversal. Biol Bull 64:424–431

    Google Scholar 

  • Glenn JD, King JG, Hillyer JF (2010) Structural mechanics of the mosquito heart and its function in bidirectional hemolymph transport. J Exp Biol 213:541–550

    PubMed  Google Scholar 

  • Grasshoff M (1968) Morphologische Kriterien als Aus-druck von Artgrenzen bei Radnetzspinnen der Subfamilie Araneinae (Arachnida, Araneae, Araneidae). Abh Senckenberg Naturforsch Ges 516:1–100

    Google Scholar 

  • Grasshoff M (1973) Bau und Mechanik der Kopulationsorgane der Radnetzspinne Mangora acalypha (Arachnida, Araneae). Z Morphol Tiere 74:241–252

    Google Scholar 

  • Griffin KJ, Stoller J, Gibson M, Chen S, Yelon D, Stainier DY, Kimelman D (2000) A conserved role for H15-related T-box transcription factors in zebrafish and Drosophila heart formation. Dev Biol 218:235–247

    PubMed  CAS  Google Scholar 

  • Grigorian M, Mandal L, Hakimi M, Ortiz I, Hartenstein V (2011) The convergence of Notch and MAPK signaling specifies the blood progenitor fate in the Drosophila mesoderm. Dev Biol 353:105–118

    PubMed  CAS  Google Scholar 

  • Gruner HE (ed) (1993) Arthropoda. In: Lehrbuch der Speziellen Zoologie. Vol. I/4. Gustav Fischer Verlag, Jena

    Google Scholar 

  • Handel K, Basal A, Fan X, Roth S (2005) Tribolium castaneum twist: gastrulation and mesoderm formation in a short-germ beetle. Dev Genes Evol 215:13–31

    PubMed  Google Scholar 

  • Hantschk A (1991) Functional morphology of accessory circulatory organs in the legs of Hemiptera. Int J Insect Morphol 20:259–274

    Google Scholar 

  • Harrison JF, Roberts SP (2000) Flight respiration and energetics. Annu Rev Physiol 62:179–205

    PubMed  CAS  Google Scholar 

  • Harrison JF, Woods HA, Roberts SP (2012) Ecological and environmental physiology of insects. Oxford University Press, Oxford

    Google Scholar 

  • Hartenstein V, Mandal L (2006) The blood/vascular system in a phylogenetic perspective. BioEssays 28:1203–1210

    PubMed  Google Scholar 

  • Harvey RP (1996) NK-2 homeobox genes and heart development. Dev Biol 178:203–216

    PubMed  CAS  Google Scholar 

  • Haupt J (1976) Die segmentalen Kopfdrüsen von Scutigerella (Symphyla, Myriapoda). Zool Beitr 22:19–37

    Google Scholar 

  • Heinrich B (1971) Temperature regulation of the sphinx moth, Manduca sexta. II. Regulation of heat loss by control of blood circulation. J Exp Biol 54:153–166

    PubMed  CAS  Google Scholar 

  • Heinrich B (1976) Heat exchange in relation to blood flow between thorax and abdomen. J Exp Biol 64:561–585

    PubMed  CAS  Google Scholar 

  • Heinrich B (1979) Keeping a cool head: honeybee thermoregulation. Science 205:1269–1271

    PubMed  CAS  Google Scholar 

  • Heinrich B (1980a) Mechanisms of body-temperature regulation in honeybees, Apis mellifera I. Regulation of head temperature. J Exp Biol 85:61–73

    Google Scholar 

  • Heinrich B (1980b) Mechanisms of body-temperature regulation in honeybees, Apis mellifera. II. Regulation of thoracic temperatures at high air temperatures. J Exp Biol 85:73–87

    Google Scholar 

  • Heinrich B (1987a) Thermoregulation by winter-flying endothermic moths. J Exp Biol 127:313–332

    Google Scholar 

  • Heinrich B (1987b) Thermoregulation in winter moths. Sci Amer 256:104–111

    Google Scholar 

  • Heinrich B (1993) The hot-blooded insects: mechanisms and evolution of thermoregulation. Harvard University Press, Cambridge

    Google Scholar 

  • Heinrich B (1996) The thermal warriors: strategies of insect survival. Harvard University Press, Cambridge

    Google Scholar 

  • Heinrich B, Bartholomew GA (1971) An analysis of pre-flight warm-up in the sphinx moth, Manduca sexta. J Exp Biol 55:223–239

    Google Scholar 

  • Heinrich B, Esch H (1994) Thermoregulation in bees. Am Sci 82:164–170

    Google Scholar 

  • Herbst C (1891) Beiträge zur Kenntnis der Chilopoden. Bibliotheca Zoologica 9:1–42

    Google Scholar 

  • Hertel W (2009) Contributions on cardiac physiology in Diplopoda (Myriapoda). Physiol Entomol 34:296–299

    Google Scholar 

  • Hertel W, Neupert S, Eckert M (2012) Proctolin in the antennal circulatory system of lower Neoptera: a comparative pharmacological and immunohistochemical study. Physiol Entomol 37:160–170

    CAS  Google Scholar 

  • Hertel W, Pass G (2002) An evolutionary treatment of the morphology and physiology of circulatory organs in insects. Comp Biochem Physiol A 133:555–575

    Google Scholar 

  • Hertel W, Pass G, Penzlin H (1985) Electrophysiological investigation of the antennal heart of Periplaneta americana and its reactions to proctolin. J Insect Physiol 31:563–572

    CAS  Google Scholar 

  • Hertel W, Rapus J, Richter M, Eckert M, Vettermann S, Penzlin H (1997) The proctolinergic control of the antenna-heart in Periplaneta americana (L.). Zoology 100:70–79

    Google Scholar 

  • Hertel W, Wirkner CS, Pass G (2002) Studies on the cardiac physiology of Onychophora and Chilopoda. Comp Biochem Physiol A 133:605–609

    CAS  Google Scholar 

  • Hessel JH (1969) The comparative morphology of the dorsal vessel and accessory structures of the Lepidoptera and its phylogenetic implications. Ann Entomol Soc Am 62:353–370

    Google Scholar 

  • Hetz SK, Psota E, Wasserthal LT (1999) Roles of aorta, ostia and tracheae in heartbeat and respiratory gas exchange in pupae of Troides rhadamantus Staudinger 1888 and Ornithoptera priamus L. 1758 (Lepidoptera, Papilionidae). Int J Insect Morphol 28:131–144

    Google Scholar 

  • Hickman V (1936) The embryology of the syncarid crustacean Anaspides tasmaniae. Pap Proc R Soc Tas 1–35

    Google Scholar 

  • Hilken G (1997) Tracheal systems in Chilopoda: a comparison under phylogenetic aspects. Entomol Scand Suppl 51:49–60

    Google Scholar 

  • Hilken G (1998) Vergleich von Tracheensystemen unter phylogenetischem Aspekt. Verh Naturwiss Vereins Hamburg (NF) 37:5–94

    Google Scholar 

  • Hilken G, Rosenberg J (2005) A new cell type associated with haemolymph vessels in the centipede Scutigera coleoptrata (Chilopoda, Notostigmophora). Entomol Gen 27:201–210

    Google Scholar 

  • Hilken G, Wirkner CS, Rosenberg J (2006) On the structure and function of the aortic diverticles in Scutigera coleoptrata (Chilopoda, Scutigeromorpha). Norw J Entomol 53:107–112

    Google Scholar 

  • Huber BA (1992) Frontal heart and arterial system in the head of Isopoda. Crustaceana 63:57–69

    Google Scholar 

  • Huber BA (1993) Genital mechanics and sexual selection in the spider Nesticus cellulanus (Araneae: Nesticidae). Can J Zool 71:2437–2447

    Google Scholar 

  • Huber BA (2004) Evolutionary transformation from muscular to hydraulic movements in spider (Arachnida, Araneae) genitalia: a study based on histological serial sections. J Morphol 261:364–376

    PubMed  Google Scholar 

  • Huckstorf K, Kosok G, Seyfarth EA, Wirkner CS (2013) The hemolymph vascular system in Cupiennius salei (Araneae: Ctenidae). Zool Anz (in press)

    Google Scholar 

  • Huckstorf K, Wirkner CS (2011) Comparative morphology of the hemolymph vascular system in krill (Euphausiacea; Crustacea). Arthropod Struc Dev 40:39–53

    Google Scholar 

  • Hustert R (1999) Accessory hemolymph pump in the mesothoracic legs of locusts (Schistocerca gregaria Forskal) (Orthoptera, Acrididae). Int J Insect Morphol 28:91–96

    Google Scholar 

  • Hustert R, Pass G (in prep) New accessory pumps for circulation in insect appendages: mechanism and neuronal drive of the cricket ovipositor-hearts

    Google Scholar 

  • Ichikawa T (2009) Mechanism of hemolymph circulation in the pupal leg of tenebrionid beetle Zophobas atratus. Comp Biochem Physiol A 153:174–180

    Google Scholar 

  • Iliadi KG, Knight D, Boulianne GL (2012) Healthy aging—insights from Drosophila. Front Physiol 3:106. doi:10.3389/fphys.2012.00106

  • Janssen R, Budd GE, Damen WG, Prpic NM (2008) Evidence for Wg-independent tergite boundary formation in the millipede Glomeris marginata. Dev Genes Evol 218:361–370

    PubMed  CAS  Google Scholar 

  • Janssen R, Damen WG (2008) Diverged and conserved aspects of heart formation in a spider. Evol Dev 10:155–165

    PubMed  CAS  Google Scholar 

  • Janssen R, Prpic NM, Damen WG (2004) Gene expression suggests decoupled dorsal and ventral segmentation in the millipede Glomeris marginata (Myriapoda: Diplopoda). Dev Biol 268:89–104

    PubMed  CAS  Google Scholar 

  • Janssen R, Prpic NM, Damen WG (2006) Dorso-ventral differences in gene expression in Glomeris marginata (Villers 1789) (Myriapoda: Diplopoda). Norw J Entomol 53:129–137

    Google Scholar 

  • Johannsen OA, Butt FH (1941) Embryology of insects and myriapods. McGraw-Hill, New York

    Google Scholar 

  • Jones JC (1977) The circulatory system of insects. Thomas, Springfield

    Google Scholar 

  • Juberthie-Jupeau L (1971) Glandes à sécrétion externe de la tête des Symphyles. Rev Écol Biol Sol 8:617–629

    Google Scholar 

  • Kihara A, Kuwasawa K (1984) A neuroanatomical and electrophysiological analysis of nervous regulation in the heart of an isopod crustacean, Bathynomus doederleini: excitatory and inhibitory junction potentials. J Comp Physiol 154:883–894

    Google Scholar 

  • Kingsley JS (1885) Notes on the embryology of Limulus. Q J Microsc Sci 25:521–576

    Google Scholar 

  • King JG, Hillyer JF (2012) Infection-induced interaction between the mosquito circulatory and immune systems. PLoS Pathogens. 8(11): e1003058

    PubMed  CAS  Google Scholar 

  • Kingsley JS (1893) The embryology of Limulus, part II. J Morphol 8:195–268

    Google Scholar 

  • Klussmann-Fricke B-J, Prendini L, Wirkner CS (2013) Evolutionary morphology of the hemolymph vascular system in scorpions: a character analysis. Arthropod Struct Dev 41:545–560

    Google Scholar 

  • Krenn HW (1993) Postembryonic development of accessory wing circulatory organs in Locusta migratoria (Orthoptera: Acrididae). Zool Anz 230:227–236

    Google Scholar 

  • Krenn HW (2010) Feeding mechanisms of adult Lepidoptera: structure, function, and evolution of the mouthparts. Annu Rev Entomol 55:307–327

    PubMed  CAS  Google Scholar 

  • Krenn HW, Pass G (1993) Wing-hearts in Mecoptera (Insecta). Int J Insect Morphol 22:63–76

    Google Scholar 

  • Krenn HW, Pass G (1994) Morphological diversity and phylogenetic analysis of wing circulatory organs in insects, part I: non-Holometabola. Zoology 98:7–22

    Google Scholar 

  • Krenn HW, Pass G (1995) Morphological diversity and phylogenetic analysis of wing circulatory organs in insects, part II: Holometabola. Zoology 98:147–164

    Google Scholar 

  • Kristensen NP (1975) The phylogeny of hexapod “orders” a critical review of recent accounts. Z Zool Syst Evol 13:1–44

    Google Scholar 

  • Kropf C (2013) Hydraulic system of locomotion. In: Nentwig W (ed) Spider ecophysiology. Springer, Heidelberg (in press)

    Google Scholar 

  • Kuramoto T, Ebara A (1984) Neurohormonal modulation of the cardiac outflow flow through the cardioarterial valve in the lobster Homarus americanus. J Exp Biol 111:123–130

    Google Scholar 

  • Kuusik A, Harak M, Hiiesaar K, Metspalu L, Tartes U (1996) Different types of external gas exchange found in pupae of greater wax moth Galleria mellonella (Lepidoptera: Pyralidae). Eur J Entomol 93:23–35

    Google Scholar 

  • Kuwasawa K, Ai H, Matsushita T (1999) Cardiac reflexes and their neural pathways in lepidopterous insects. Comp Biochem Physiol A 124:581–586

    Google Scholar 

  • Lamoral BH (1973) On the morphology, anatomy, histology and function of the tarsal organ on the pedipalpi of Palystes castaneus (Sparassidae, Araneidae). Ann Natal Mus 21:609–648

    Google Scholar 

  • Lane NJ, Harrison JB, Bowermann RF (1981) A vertebrate-like blood brain barrier, with intraganglionic blood channels and occluding junctions in the scorpion. Tissue Cell 13:557–576

    PubMed  CAS  Google Scholar 

  • Lankester ER (1881) Limulus an arachnid. Q J Microsc Sci 21:504–548

    Google Scholar 

  • Lee W-K, Socha JJ (2009) Direct visualization of hemolymph flow in the heart of a grasshopper (Schistocerca americana). BMC Physiol 9:2. doi:10.1186/1472-6793-9-2

  • Lehmacher C, Abeln B, Paululat A (2012) The ultrastructure of Drosophila heart cells. Arthropod Struct Dev 41:459–474

    PubMed  Google Scholar 

  • Lehmacher C, Tögel M, Pass G, Paululat A (2009) The Drosophila wing hearts consist of syncytial muscle cells that resemble adult somatic muscles. Arthropod Struct Dev 38:111–123

    PubMed  CAS  Google Scholar 

  • Leiber G (1935) Beiträge zur vergleichenden Anatomie des Gefäßsystems der Diplopoden. Zool Jahrb Anat Ontog Tiere 59:333–354

    Google Scholar 

  • Leyton RA, Sonnenblick EH (1971) Cardiac muscle of the horseshoe crab, Limulus polyphemus I. Ultrastructure. J Cell Biol 48:101–119

    PubMed  CAS  Google Scholar 

  • Lovato TL, Nguyen TP, Molina MR, Cripps RM (2002) The Hox gene abdominal-a specifies heart cell fate in the Drosophila dorsal vessel. Development 129:5019–5027

    PubMed  CAS  Google Scholar 

  • Lowe E (1935) On the anatomy of a marine copepod, Calanus finmarchicus (Gunner). Trans R Soc Edinb 58:561–603

    Google Scholar 

  • Makioka T (1988) Internal morphology. In: Sekiguchi K (ed) Biology of horseshoe crabs. Science House, Tokyo, pp 104–132

    Google Scholar 

  • Mangum CP, Scott JL, Black REL, Miller KI, Van Holde KE (1985) Centipedal haemocyanin: its structure and its implication for arthropod phylogeny. Proc Natl Acad Sci USA 82:3721–3725

    PubMed  CAS  Google Scholar 

  • Manton SM (1928) On the embryology of a mysid crustacean, Hemimysis lamornae. Phil Trans R Soc B 216:363–463

    Google Scholar 

  • Manton SM (1934) On the embryology of the crustacean Nebalia bipes. Phil Trans R Soc B 223:163–238

    Google Scholar 

  • Matus S, Pass G (1999) Antennal circulatory organ of Apis mellifera L. (Hymenoptera: Apidae) and other Hymenoptera: functional morphology and phylogenetic aspects. Int J Insect Morphol 28:97–109

    Google Scholar 

  • Mayer G, Ruhberg H, Bartolomaeus T (2004) When the epithelium ceases to exist - an ultrastructural study on the fate of the embryonic coelom in Epiperipatus biolleyi (Onychophora, Peripatidae). Acta Zool 85:163–170

    Google Scholar 

  • Maynard DM (1960) Circulation and heart function. In: Waterman TH (ed) The physiology of Crustacea. Academic, New York, pp 161–226

    Google Scholar 

  • Mayrat A, McMahon BR, Tanaka K (2006) The circulatory system. In: Forest J, von Vaupel Klein JC, Schram FR (eds) Treatise on zoology—Anatomy, taxonomy, biology. The Crustacea revised and updated from the Traité de Zoologie, vol 2. Brill, Leiden, pp 3–84

    Google Scholar 

  • McGaw IJ (2005) The decapod crustacean circulatory system: a case that is neither open nor closed. Microsc Microanal 11:18–36

    PubMed  CAS  Google Scholar 

  • McMahon BR (2001) Control of cardiovascular function and its evolution in Crustacea. J Exp Biol 204:923–932

    PubMed  CAS  Google Scholar 

  • McMahon BR (2012) Comparative evolution and design in non-vertebrate cardiovascular systems. In: Sedmera D, Wang T (eds) Ontogeny and phylogeny of the vertebrate heart. Springer, New York, pp 1–33

    Google Scholar 

  • McMahon BR, Burnett BR (1990) The crustacean open circulatory system: a reexamination. Physiol Zool 63:35–71

    Google Scholar 

  • McMahon BR, Smith PJS, Wilkens JL (1997) Invertebrate circulatory systems. In: Danzler WH (ed) Handbook of physiology. Comparative physiology, Sect 13. American Physiological Society, New York, pp 931–1008

    Google Scholar 

  • McMahon BR, Tanaka K, Doyle JE, Chu KH (2002) A change of heart: cardiovascular development in the shrimp Metapenaeus ensis. Comp Biochem Physiol A: Mol Integr Physiol 133:577–587

    CAS  Google Scholar 

  • Meek WJ (1909) Structure of Limulus heart muscle. Amer J Physiol 20:403–412

    Google Scholar 

  • Meyer E (1931) Über den Blutkreislauf der Epheme-riden. Zeitschr Morphol Ökol Tiere 22:1–52

    Google Scholar 

  • Midttun B (1977) Ultrastructure of cardiac muscle of Trochosa terricola Thor, Pardosa amentata Clerck, P. pullata Clerck, and Pisaura mirabilis Clerck (Araneae: Lycosidae, Pisauridae). Cell Tissue Res 181:299–310

    PubMed  CAS  Google Scholar 

  • Miller TA (1985) Structure and physiology of the circulatory system. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology, biochemistry and pharmacology, vol 3. Pergamon Press, Oxford, pp 289–353

    Google Scholar 

  • Miller TA (1997) Control of circulation in insects. Gen Pharmacol 29:23–38

    PubMed  CAS  Google Scholar 

  • Miller T, Pass G (2009) Circulatory system In: Resh VH, Cardé RT (eds) Encyclopedia of insects, 2nd ed. Elsevier, Burlington, pp 169–173

    Google Scholar 

  • Milne-Edwards A (1872) Recherches sur l’anatomie des Limules. Ann Sci Nat Zool 17:1–67

    Google Scholar 

  • Monier B, Astier M, Semeriva M, Perrin L (2005) Steroid-dependent modification of Hox function drives myocyte reprogramming in the Drosophila heart. Development 132:5283–5293

    PubMed  CAS  Google Scholar 

  • Monier B, Tevy MF, Perrin L, Capovilla M, Semeriva M (2007) Downstream of homeotic genes: in the heart of hox function. Fly 1:59–67

    PubMed  Google Scholar 

  • Moreau R (1974) Variations de la pression interne au cours de 1′émergence et de l′expansion des ailes chez Bombyx mori et Pieris brassicae. J lnsect Physiol 20:1475–1480

    CAS  Google Scholar 

  • Moreau R, Lavenseau L (1975) Rôle des organes pulsatiles thoraciques et du coeur pendant l’émergence et l’expansion des ailes des Lépidoptères. J Insect Physiol 21:1531–1534

    Google Scholar 

  • Murray JA (1967) Morphology of the cercus in Blattella germanica (Blattaria: Pseudomopinae). Ann Entomol Soc Am 60:10–16

    Google Scholar 

  • Nair SG (1956) On the embryology of the isopod Irona. J Embryol Exp Morphol 4:1–33

    Google Scholar 

  • Nicolson SW (1976) Diuresis in the cabbage white butterfly Pieris brassicae: fluid excretion by the malpighian tubules. J lnsect Physiol 22:1347–1356

    CAS  Google Scholar 

  • Nigmann M (1908) Anatomie und Biologie von Acentropus niveus Oliv. Zool Jahrb Syst 26:489–560

    Google Scholar 

  • Nishimura M, Ocorr K, Bodmer R, Cartry J (2011) Drosophila as a model to study cardiac aging. Exp Gerontol 46:326–330

    PubMed  CAS  Google Scholar 

  • Nutting WL (1951) A comparative anatomical study of the heart and accessory structures of the orthopteroid insects. J Morphol 89:501–597

    Google Scholar 

  • Ocorr K, Akasaka T, Bodmer R (2007) Age-related cardiac disease model of Drosophila. Mech Ageing Dev 128:112–116

    PubMed  CAS  Google Scholar 

  • Økland S, Tjønneland A, Nylund A, Larsen LN, Christ I (1982) The membrane systems and the sarcomere in the heart of Lithobius forficatus L. (Arthropoda, Chilopoda). Zool Anz 208:124–131

    Google Scholar 

  • Ono M, Igarashi T, Ohno E, Sasaki M (1995) Unusual thermal defense by a honeybee against mass attack by hornets. Nature 377:334–336

    CAS  Google Scholar 

  • Parry DA, Brown RHJ (1959) The jumping mechanism of salticid spiders. J Exp Biol 36:654–664

    Google Scholar 

  • Pass G (1980) The anatomy and ultrastructure of the antennal circulatory organs in the cockchafer beetle Melolontha melolontha L. (Coleoptera, Scarabaeidae). Zoomorphology 96:77–89

    Google Scholar 

  • Pass G (1985) Gross and fine structure of the antennal circulatory organ in cockroaches (Blattodea, Insecta). J Morphol 185:255–268

    Google Scholar 

  • Pass G (1987) The “cercus heart” in stoneflies—a new type of accessory circulatory organ in insects. Naturwiss 74:440–441

    Google Scholar 

  • Pass G (1988) Functional morphology and evolutionary aspects of unusual antennal circulatory organs in Labidura riparia Pallas (Labiduridae), Forficula auricularia L. and Chelidurella acanthopygia Géné (Forficulidae) (Dermaptera: Insecta). Int J Insect Morphol 17:103–112

    Google Scholar 

  • Pass G (1991) Antennal circulatory organs in Onychophora, Myriapoda and Hexapoda: functional morphology and evolutionary implications. Zoomorphology 110:145–164

    Google Scholar 

  • Pass G (1998) Accessory pulsatile organs. In: Harrison F, Locke M (eds) Microscopic anatomy of invertebrates, vol 11B. Wiley-Liss, New York, pp 621–640

    Google Scholar 

  • Pass G (2000) Accessory pulsatile organs: evolutionary innovations in insects. Annu Rev Entomol 45:495–518

    PubMed  CAS  Google Scholar 

  • Pass G, Agricola H, Birkenbeil H, Penzlin H (1988a) Morphology of neurones associated with the antennal heart of Periplaneta americana (Blattodea, Insecta). Cell Tissue Res 253:319–326

    PubMed  CAS  Google Scholar 

  • Pass G, Gereben-Krenn B-A, Merl M, Plant J, Szucsich NU, Tögel M (2006) Phylogenetic relationships of the orders of Hexapoda: Contributions from the circulatory organs for a morphological data matrix. Arthr Syst Phyl 64:165–203

    Google Scholar 

  • Pass G, Sperk G, Agricola H, Baumann E, Penzlin H (1988b) Octopamine in a neurohaemal area within the antennal heart of the American cockroach. J Exp Biol 135:495–498

    CAS  Google Scholar 

  • Paul R, Bihlmayer S (1995) Circulatory physiology of a tarantula (Eurypelma californicum). Zoology 98:69–81

    Google Scholar 

  • Paul R, Bihlmayer S, Colmorgan M, Zahler S (1994) The open circulatory system of spiders (Eurypelma californicum, Pholcus phalangoides): A survey of functional morphology and physiology. Physiol Zool 67:1360–1382

    Google Scholar 

  • Perrin L, Monier B, Ponzielli R, Astier M, Semeriva M (2004) Drosophila cardiac tube organogenesis requires multiple phases of Hox activity. Dev Biol 272:419–431

    PubMed  CAS  Google Scholar 

  • Pigliucci M, Müller GB (2010) Evolution: the extended synthesis. MIT Press, Cambridge

    Google Scholar 

  • Pirow R, Wollinger F, Paul RJ (1999) The sites of respiratory gas exchange in the planktonic crustacean Daphnia magna: an in vivo study employing blood haemoglobin as an internal oxygen probe. J Exp Biol 202:3089–3099

    PubMed  Google Scholar 

  • Ponzielli R, Astier M, Chartier A, Gallet A, Therond P, Semeriva M (2002) Heart tube patterning in Drosophi-la requires integration of axial and segmental information provided by the Bithorax complex genes and hedgehog signaling. Development 129:4509–4521

    PubMed  CAS  Google Scholar 

  • Price AL, Patel NH (2008) Investigating divergent mechanisms of mesoderm development in arthropods: the expression of Ph-twist and Ph-mef2 in Parhyale hawaiensis. J Exp Zool B 310:24–40

    Google Scholar 

  • Prpic NM (2004) Homologs of wingless and decapentaplegic display a complex and dynamic expression profile during appendage development in the millipede Glomeris marginata (Myriapoda: Diplopoda). Front Zool 1:6. doi:10.1186/1742-9994-1-6

  • Prpic NM, Janssen R, Damen WG, Tautz D (2005) Evolution of dorsal-ventral axis formation in arthropod appendages: H15 and optomotor-blind/bifid-type T-box genes in the millipede Glomeris marginata (Myriapoda: Diplopoda). Evol Dev 7:51–57

    PubMed  CAS  Google Scholar 

  • Raina A, Meola S, Wergin W, Blackburn M, Bali G (2003) Antennal ampullary glands of Helicoverpa zea (Lepidoptera: Noctuidae). Cell Tissue Res 312:127–134

    PubMed  Google Scholar 

  • Rajulu G (1967) Physiology of the heart of Cingalobolus bugnioni (Diplopoda: Myriapoda). Cell Mol Life Sci 23:388

    CAS  Google Scholar 

  • Rajulu GS (1969) Presence of haemocyanin in the blood of a centipede Scutigera longicornis (Chilopoda: Myriapoda). Curr Sci India 38:168–169

    CAS  Google Scholar 

  • Randall WC (1966) Microanatomy of the heart and associated structures of two scorpions, Centruroides sculpturatus Ewing and Uroctonus mordax Thorell. J Morphol 119:161–180

    PubMed  CAS  Google Scholar 

  • Redmond JR, Jorgensen DD, Bourne GB (1982) Circulatory physiology of Limulus. Prog Clin Biol Res 81:133–146

    PubMed  CAS  Google Scholar 

  • Reiber CL, McGaw IJ (2009) A review of the “open” and “closed” circulatory systems: new terminology for complex invertebrate circulatory systems in light of current findings. Int J Zool. doi:10.1155/2009/301284

    Google Scholar 

  • Reim I, Frasch M (2010) Genetic and genomic dissection of cardiogenesis in the Drosophila model. Pediatr Cardiol 31:325–334

    PubMed  Google Scholar 

  • Richards AG (1963) The ventral diaphragm of insects. J Morphol 113:17–47

    Google Scholar 

  • Rilling G (1968) Großes zoologisches Praktikum. Teil 13b: Lithobius forficatus. Gustav Fischer, Stuttgart

    Google Scholar 

  • Ryan KM, Hoshizaki DK, Cripps RM (2005) Homeotic selector genes control the patterning of seven-up expressing cells in the Drosophila dorsal vessel. Mech Dev 122:1023–1033

    PubMed  CAS  Google Scholar 

  • Saalfeld E (1936) Untersuchungen über den Blutkreislauf bei Leptodora hyalina. Z vergl Physiol 24:58–70

    Google Scholar 

  • Sandeman DC (1967) The vascular circulation in the brain, optic lobes and thoracic ganglia of the crab Carcinus. Proc R Soc B 168:82–90

    CAS  Google Scholar 

  • Schneider D, Kaissling KE (1959) Der Bau der Antenne des Seidenspinners Bombyx mori L. III. Das Bindegewebe und das Blutgefäß. Zool Jahrb Anat Ontog 77:111–132

    Google Scholar 

  • Scholl G (1963) Embryologische Untersuchungen an Tanaidaceen (Heterotanais oerstedi Kroyer). Zool Jahrb Anat Ontog 80:500–554

    Google Scholar 

  • Scholl G (1977) Beitrage zur Embryonalentwicklung von Limulus polyphemus L. (Chelicerata, Xiphosura). Zoomorphologie 86:99–154

    Google Scholar 

  • Scholtz G, Kamenz C (2006) The book lungs of Scorpiones and Tetrapulmonata (Chelicerata, Arachnida): evidence for homology and a single terrestrialisation event of a common arachnid ancestor. Zoology 109:2–13

    PubMed  Google Scholar 

  • Seifert B (1932) Anatomie und Biologie des Diplopoden Strongylosoma pallipes Oliv. Zoomorphology 25:362–507

    Google Scholar 

  • Seifert G, Rosenberg J (1978) Feinstruktur der Herzwand des Doppelfüßers Oxidus gracilis (Diplopoda: Paradoxosomatidae) und allgemeine Betrachtungen zum Aufbau der Gefäße von Tracheata und Onychophora. Entomol Gener 4:224–233

    Google Scholar 

  • Selman BJ (1965) The circulatory system of the alder fly Sialis lutaria. Proc Zool Soc Lond 144:487–535

    Google Scholar 

  • Sherman RG (1985) Neural control of the heartbeat and skeletal muscle in spiders and scorpions. In: Barth FG (ed) Neurobiology of arachnids. Springer, New York, pp 319–336

    Google Scholar 

  • Sherman RG, Bursey CR, Fourtner CR, Pax RA (1969) Cardiac ganglia in spiders (Arachnida, Araneae). Experientia 25:438

    PubMed  CAS  Google Scholar 

  • Shubin N, Tabin C, Carroll S (2009) Deep homology and the origins of evolutionary novelty. Nature 457:818–823

    PubMed  CAS  Google Scholar 

  • Siewing R (1954) Über die Verwandtschaftsbeziehungen der Anaspidaceen. Verh Deutsch Zool Ges 210–252

    Google Scholar 

  • Siewing R (1956) Untersuchungen zur Morphologie der Malacostraca (Crustacea). Zool Jahrb Anat Ontog Tiere 75:39–176

    Google Scholar 

  • Siewing R (1959) Syncarida. In: Gruner H-E (ed) Bronn’s Klassen und Ordnungen des Tierreichs, vol 5., 1. Abteilung, Akademische Verlagsgesellschaft Geest & Portig, Leipzig, pp 1–121

    Google Scholar 

  • Siewing R (1969) Lehrbuch der vergleichenden Entwicklungsgeschichte der Tiere. Paul Parey, Hamburg

    Google Scholar 

  • Silen L (1954) On the circulatory system of the Isopoda Oniscoidea. Acta Zool 35:11–70

    Google Scholar 

  • Sláma K (1999) Active regulation of insect respiration. Ann Entomol Soc Am 92:916–929

    Google Scholar 

  • Sláma K (2000) Extracardiac versus cardiac haemocoelic pulsations in pupae of the mealworm (Tenebrio molitor L.). J Insect Physiol 46:977–992

    PubMed  Google Scholar 

  • Sláma K (2008) Extracardiac haemocoelic pulsations and the autonomic neuroendocrine system (coelopulse) of terrestrial insects. Terr Arthrop Rev 1:39–80

    Google Scholar 

  • Sláma K (2010) Physiology of heartbeat reversal in adult Drosophila melanogaster (Diptera: Drosophilidae). Eur J Entomol 107:13–31

    Google Scholar 

  • Sláma K, Baudry-Partiaogolou N, Provansal-Baudez A (1979) Control of extracardiac haemolymph pressure pulses in Tenebrio molitor. J Insect Physiol 25:825–831

    Google Scholar 

  • Sláma K, Farkas R (2005) Heartbeat patterns during the postembryonic development of Drosophila melanogaster. J Insect Physiol 51:489–503

    PubMed  Google Scholar 

  • Sláma K, Neven L (2001) Active regulation of respiration and circulation in pupae of the codling moth (Cydia pomonella). J Insect Physiol 47:1321–1336

    PubMed  Google Scholar 

  • Steinacker A (1978) The anatomy of the decapod crustacean auxiliary heart. Biol Bull 154:497–507

    PubMed  CAS  Google Scholar 

  • Steinacker A (1979) Neural and neurosecretory control of the decapod crustacean auxiliary heart. Am Zool 19:67–75

    Google Scholar 

  • Storch V, Ruhberg H (1993) Onychophora. In: Harrison FW, Rice ME (eds) Microscopic anatomy of invertebrates, vol 12. Wiley-Liss, New York, pp 11–56

    Google Scholar 

  • Sun BD, Schmidt JM (1997) The structure of the antennal heart of Aedes aegypti (Linnaeus). Can J Zool 75:444–458

    Google Scholar 

  • Tao Y, Schulz RA (2007) Heart development in Drosophila. Semin Cell Dev Biol 18:3–15

    PubMed  CAS  Google Scholar 

  • Tartes U, Vanatoa A, Kuusik A (2002) The insect abdomen: a heartbeat manager in insects? Comp Biochem Physiol A 133:611–623

    CAS  Google Scholar 

  • Tauc HM, Mann T, Werner K, Pandur P (2012) A role for Drosophila Wnt-4 in heart development. Genesis 50:466–481

    PubMed  CAS  Google Scholar 

  • Tiegs OW (1940) The embryology and affinities of the Symphyla, based on a study of Hanseniella agilis. Q J Microsc Sci 82:1–225

    Google Scholar 

  • Tiegs OW (1945) The post-embryonic development of Hanseniella agilis (Symphyla). Q J Microsc Sci 85:191–328

    Google Scholar 

  • Tjønneland A, Kryvi H, Ostnes JP, Økland S (1985a) The heart ultrastructure in two species of pycnogonids and its phylogenetic implications. Zool Scr 14:215–219

    Google Scholar 

  • Tjønneland A, Økland S, Midttun B (1985b) Myocardial ultrastructure in five species of scorpions (Chelicerata). Zool Anz 214:7–17

    Google Scholar 

  • Tögel M, Pass G, Paululat A (2008) The Drosophila wing hearts originate from pericardial cells and are essential for wing maturation. Dev Biol 318:29–37

    PubMed  Google Scholar 

  • Vogt G, Wirkner CS, Richter S (2009) Symmetry variation in the heart-descending artery system of the parthenogenetic marbled crayfish. J Morphol 207:221–226

    Google Scholar 

  • Wägele JW (1992) Isopoda. In: Harrison FW, Humes AG (eds) Microscopic anatomy of invertebrates, vol 9. Wiley-Liss, New York, pp 529–617

    Google Scholar 

  • Wagenseil JE, Mecham RP (2009) Vascular extracellular matrix and arterial mechanics. Physiol Rev 89:957–989

    PubMed  CAS  Google Scholar 

  • Walker G (1991) Cirripedia. In: Harrison FW, Humes AG (eds) Microscopic anatomy of invertebrates, vol 9. Wiley-Liss, New York, pp 225–311

    Google Scholar 

  • Wasserthal LT (1975) Periodische Herzschlag-Umkehr bei Insekten. Umschau 75:93–94

    Google Scholar 

  • Wasserthal LT (1980) Oscillating haemolymph “circulation” in the butterfly Papilio machaon L. revealed by contact thermography and photocell measurements. J Comp Physiol 139:145–163

    Google Scholar 

  • Wasserthal LT (1996) Interaction of circulation and tracheal ventilation in holometabolous insects. Adv Insect Physiol 26:297–351

    Google Scholar 

  • Wasserthal LT (1998) The open hemolymph system of Holometabola and its relation to the tracheal space. In: Harrison F, Locke M (eds) Microscopic anatomy of invertebrates, vol 11B. Wiley-Liss, New York, pp 583–620

    Google Scholar 

  • Wasserthal LT (1999) 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. Int J Insect Morphol 28:111–129

    Google Scholar 

  • Wasserthal LT (2003a) Hämolymphe und Hämolymphtransport. In: Dettner K, Peters W (eds) Lehrbuch der Entomologie, 2nd edn. Spektrum, Heidelberg, pp 185–203

    Google Scholar 

  • Wasserthal LT (2003b) Respiration. In: Kristensen NP (ed) Handbook of zoology, vol 4/36–2. Lepidoptera. de Gruyter, Berlin, pp 189–203

    Google Scholar 

  • Wasserthal LT (2003c) Circulation and thermoregulation. In: Kristensen NP (ed) Handbook of zoology, vol 4/36-2. Lepidoptera. de Gruyter, Berlin, pp 205–228

    Google Scholar 

  • Wasserthal LT (2007) Drosophila flies combine periodic heartbeat reversal with a circulation in the anterior body mediated by a newly discovered anterior pair of ostial valves and ‘venous’ channels. J Exp Biol 210:3707–3719

    PubMed  Google Scholar 

  • Wasserthal LT (2012) Influence of periodic heartbeat reversal and abdominal movements on hemocoelic and tracheal pressure in resting blowflies Calliphora vicina. J Exp Biol 215:362–373

    PubMed  Google Scholar 

  • Watson WH, Groome JR (1989) Modulation of Limulus heart. Am Zool 29:1287–1303

    Google Scholar 

  • Weber H (1954) Grundriß der Insektenkunde. 3. Aufl. Gustav Fischer, Stuttgart

    Google Scholar 

  • West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University Press, New York

    Google Scholar 

  • Weygoldt P (1961) Beitrag zur Kenntnis der Ontogenie der Dekapoden: embryologische Untersuchungen an Palaemonetes varians (Leach). Zool Jahrb Anat Ontog 79:223–294

    Google Scholar 

  • Weygoldt P (1975) Untersuchungen zur Embryologie und Morphologie der Geißelspinne Tarantula marginemaculata C.L.Koch (Arachnida, Amblypygi, Tarantulidae). Zoomorphologie 82:137–199

    Google Scholar 

  • Whedon A (1938) The aortic diverticula of the Odonata. J Morphol 63:229–261

    Google Scholar 

  • Wilkens JL, Cavey MJ, Shovkivska I, Zhang ML, ter Keurs HEDJ (2008) Elasticity, unexpected contractility and the identification of actin and myosin in lobster arteries. J Exp Biol 21:766–772

    Google Scholar 

  • Wilkens JL, Davidson GW, Cavey MJ (1997a) Vascular peripheral resistance and compliance in the lobster Homarus americanus. J Exp Biol 200:477–485

    PubMed  Google Scholar 

  • Wilkens JL, Walker RL (1992) Nervous control of crayfish cardiac hemodynamics. Comp Physiol 11:115–122

    Google Scholar 

  • Wilkens JL, Yazawa T, Cavey MJ (1997b) Evolutionary derivation of the American lobster cardiovascular system: an hypothesis based on morphological and physiological evidence. Invertebr Biol 116:30–38

    Google Scholar 

  • Wirkner CS, Hilken G, Rosenberg J (2011) The circulatory system. In: Minelli A (ed) Treatise on zoology—anatomy, taxonomy, biology, vol 1., Myriapoda. Brill, Leiden, pp 157–176

    Google Scholar 

  • Wirkner CS, Pass G (2002) The circulatory system in Chilopoda: functional morphology and phylogenetic aspects. Acta Zool 83:193–202

    Google Scholar 

  • Wirkner CS, Prendini L (2007) Comparative morphology of the hemolymph vascular system in scorpions—a survey using corrosion casting, MicroCT, and 3D-reconstruction. J Morphol 268:401–413

    PubMed  Google Scholar 

  • Wirkner CS, Richter S (2003) The circulatory system in Phreatoicidea: implications for the isopod ground pattern and peracarid phylogeny. Arthropod Struct Dev 32:337–347

    PubMed  CAS  Google Scholar 

  • Wirkner CS, Richter S (2004) Improvement of microanatomical research by combining corrosion casts with MicroCT and 3D reconstruction, exemplified in the circulatory organs of the woodlouse. Microsc Res Tech 64:250–254

    PubMed  Google Scholar 

  • Wirkner CS, Richter S (2007a) Comparative analysis of the circulatory system in Amphipoda (Malacostraca, Crustacea). Acta Zool 88:159–171

    Google Scholar 

  • Wirkner CS, Richter S (2007b) The circulatory system and its spatial relations to other major organ systems in Spelaeogriphacea and Mictacea (Malacostraca, Crustacea)—a three-dimensional analysis. Zool J Linn Soc 149:629–642

    Google Scholar 

  • Wirkner CS, Richter S (2007c) The circulatory system in Mysidacea—Implications for the phylogenetic position of Lophogastrida and Mysida (Malacostraca, Crustacea). J Morphol 268:311–328

    PubMed  Google Scholar 

  • Wirkner CS, Richter S (2008) Morphology of the haemolymph vascular system in Tanaidacea and Cumacea: Implications for the relationships of “core group” Peracarida (Malacostraca; Crustacea). Arthropod Struct Dev 37:141–154

    PubMed  Google Scholar 

  • Wirkner CS, Richter S (2009) The hemolymph vascular system in Tethysbaena argentarii (Thermosbaenacea, Monodellidae) as revealed by 3D reconstruction of semi-thin sections. J Crust Biol 29:13–17

    Google Scholar 

  • Wirkner CS, Richter S (2010) Evolutionary morphology of the circulatory system in Peracarida (Malacostraca; Crustacea). Cladistics 26:143–167

    Google Scholar 

  • Wirkner CS, Richter S (2013) Circulatory system and respiration. In: Thiel M, Watling L (eds) The natural history of the Crustacea, vol 1. Oxford University Press, Oxford, pp 376–412

    Google Scholar 

  • Wolf MJ, Amrein H, Izatt JA, Choma MA, Reedy MC, Rockman HA (2006) Drosophila as a model for the identification of genes causing adult human heart disease. Proc Natl Acad Sci USA 103:1394–1399

    PubMed  CAS  Google Scholar 

  • Xavier-Neto J, Davidson B, Simoes-Costa MS, Castro RA, Castillo HA, Sampaio AC (2010) Evolutionary origins of hearts. In: Rosenthal N, Harvey RP (eds) Heart development and regeneration. Elsevier, London, pp 3–46

    Google Scholar 

  • Yamagishi H, Ando H, Makioka T (1997) Myogenic heartbeat in the primitive crustacean Triops longicaudatus. Biol Bull 193:350–358

    Google Scholar 

  • Yamazaki K, Akiyama-Oda Y, Oda H (2005) Expression patterns of a twist-related gene in embryos of the spider Achaearanea tepidariorum reveal divergent aspects of mesoderm development in the fly and spider. Zool Sci 22:177–185

    PubMed  CAS  Google Scholar 

  • Zaffran S, Frasch M (2002) Early signals in cardiac development. Circ Res 91:457–469

    PubMed  CAS  Google Scholar 

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Acknowledgments

Cordial thanks to John Plant and Lucy Cathrow for the linguistic revision of the manuscript, and Torben Göpel for technical assistance. We thank Heidemarie Grillitsch for drawing of some graphs and Bastian-Jesper Klussmann-Fricke (University Rostock) for a photograph. CSW thanks all members of his lab for discussions and technical help. The work was supported by the German Research Foundation (DFG) 3334/1-2, 3334/3-1, 3334/4-1 (C.S.W) and the Austrian Science Fund P23251 (G.P. and M.T.).

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  1. Allgemeine und Spezielle Zoologie, Universität Rostock, Universitätsplatz 2, 18055, Rostock, Germany

    Christian S. Wirkner

  2. Department of Integrative Zoology, University of Vienna, Althanstraße 14, 1090, Vienna, Austria

    Markus Tögel & Günther Pass

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  1. Christian S. Wirkner
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Correspondence to Christian S. Wirkner .

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  1. , Department of Biology, University of Padova, Via Ugo Bassi 58 B, Padova, 35131, Italy

    Alessandro Minelli

  2. , Zoology Department, Natural History Museum, London, SW7 5BD, United Kingdom

    Geoffrey Boxshall

  3. , Department of Biology, University of Padova, Via Ugo Bassi 58 B, Padova, 35131, Italy

    Giuseppe Fusco

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Wirkner, C.S., Tögel, M., Pass, G. (2013). The Arthropod Circulatory System. In: Minelli, A., Boxshall, G., Fusco, G. (eds) Arthropod Biology and Evolution. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-36160-9_14

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