S. Afr. 1 Zool. 1998,33(2) 87-106

Integration of physiological responses of crustaceans to environmental challenge

SIeve Morris' and Chris N. Airriess" School of Biological Sciences, University of Sydney, Sydney, NSW 2006, Australia. E-mail: [email protected]

Received 2 September 1997; accepted 17 April/998

Brachyuran crustaceans are useful models for physiological studies because of their intermediate size and since they occupy a spectrum of habitats requiring widety varied behaviour. In this paper we examine the physi­ ological responses to environmental fluctuations, extremes of habitat and consequent behaviours, with special emphasis on the adoption of air-breathing. It is established that metabolic end products such as lactate, interme­ diates including urate, and monoamine and peptide neurohormones can have important regulatory roles. These include effects on ventilation and heart function, blood perfusion, respiratory gas transport, as well as water and salt homeostasis providing an integrated suite of control mechanisms to regulate responses to environmental or behaviourally induced stress. A separate body of work has long suggested that the regulation of energy metab­ olism and provision of metabolic fuel for glycotysis is influenced by similar effectors. Most recently, metabolic end-products have been implicated as effectors of behaviour and thereby metabolic state. Thus, there is strong, emerging evidence for integration of physiological control mechanisms at the organismallevel. We present new information, both mechanistic and from eco-physiologicallaboratory simulations, and from field studies of terres­ trial crabs, that strengthens and extends the scope of this integration. Branchial chamber ventilation, cardiovas­ cular function, relative perfusion of gills v. lungs, gas transport in the blood, the mobilisation of energy reserves, ion transport and water balance are all apparently influenced by similar messengers which coordinate and opti­ mise these functions to meet specific requirements .

• To whom correspondence should be addressed ··Current address: Department of Zoology, University of British Columbia, 6270 University Boulevard, Vancouver, Be, Canada V6T IZ4. E-mail: [email protected]

I ntrod uction water, and from water to land, requires significant adaptations .

) and changes in the control of water and salt balance. The ideal 9 The integration of physiological function is essential to the 0 nature of crustaceans for experimental physiology notwith­ 0 lives of all animals. To accomplish the most seemingly sim­ 2

standing, this is perhaps the most eco-physiologically diverse

d ple process a large number of physiological control mecha­ e and rewarding group of animals available to the comparative t nisms must be regulated in a manner consistent with the a and evolutionary physiologist. d current demands placed on an organism. The integration of (

The objective of this review is to illustrate by example the r physiological processes must be sufficiently sophisticated e wealth and the breadth of information available on physiolog­ h and plastic to respond to a range of behavioural and environ­ s i ical control in crustaceans. Furthermore, to go beyond this to l mental challenges. Loss of regulation, usually by failure of b illustrate how these disparate data might be brought together u part of the integrated response under extreme conditions, P

to give a more complete picture of (a) how these physiologi­

e leads to increasing physiological disturbance and ultimately

h cal responses can be integrated with respect to both environ­ t

death. mental and behavioural challenges to physiological proces­ y b Crustaceans provide an important and valuable study ses, and (b) how much more must yet be determined. Future d e model for investigation of regulation and integration in physi­ work clearly must integrate biochemistry, cell biology and t n ology. These animals occupy a large range of available habi­ ecology into the physiology of the animals, some directions to a r tats, from abyssal ocean to montane terrestrial, and thus

g which are outlined in this review.

e exhibit a plethora of adaptations to environment. The central Integration of the control of physiological responses c n nervous system (CNS) is sophisticated enough to allow gen­ requires a range of receptors (external and internal) via which e c i eration of general animal models but discrete enough to facil­

l signals can be transduced to a variety of diverse end effects.

r itate experimentation. Similarly, the complex but accessible The CNS is, by definition, paramount in physiological inte­ e d nature of the respiratory and the cardiovascular systems gration but a detailed examination of the CNS is outside the n

u encourages study of their control mechanisms and integration scope of this review. The interface between primary (intercel­ y in responding to stress. Amphibious and terrestrial crusta­ a lular) and secondary (intracellular) messengers in cell-com­ w ceans possess both lungs and gills, permitting investigation of munication systems is a pivotal aspect to address. This review e t

a physiological integration with twin gas exchange organs and is thus primarily concerned with the suite of physiological G

during the transition between water and air-breathing. Crusta­ mechanisms which respond to, and are potentially controlled t e ceans are special amongst the invertebrates in that energy by, signalling molecules transported in the haemolymph and n i metabolism during anaerobiosis is similar to that of verte­ second messenger cascades within target cells (Figure 1). b a brates during stress and results in lactacidosis. They possess a Among the putative primary messengers are biogenic neu­ S

y sophisticated respiratory gas transport pigment, regulated by roamines and peptide hormones. However, intermediate and b a suite of modulators. The transition from seawater to fresh terminal metabolites are increasingly appreciated to be d e c u d o r p e R 88 S. Afr. J. Zool. 1998,33(2)

-- - .,------",,~ -- --, the volume of study the suggestion that intracellular concen­ trations of cAMP, cGMP and IP) are modified by activation of G-protein linked receptors, thus regulating cellular responses to neuroamines and pep tides, remains undemon­ SENSORY I~. r".,TC­ ===:>1, strated in all but a few cases. INPUTS Another level of integration of physiological function, which will be considered in some detail in the relation to metabolism, oxygen delivery and thennoregulation, involves the role of metabolic intennediates and end-products as inter­ cellular messengers. This is a conceptually very different sys­ r­ tem, where compounds such as glucose, urate and lactate I I arising from metabolic processes can influence other physio­ I logical and behavioural response systems-an 'autoregula­ I I tion' of soMs. I cAMP Experimentally, hypoxia, exercise, and changes in temper­ I Mediated ature and salinity are frequently applied challenges and, therefore, are widely used in interpretation of physiological capability. The literature provides material on the regulation • ~ HAEMOLYMPH I .. of respiratory gas exchange, modification of cardiovascular I" t ____~ responses, the provision of metabolic fuels, the maintenance I"" '~ of salt and water balance and the inter-dependence ofphysiol­ :~ :~ ogy and behaviour. Additionally, circadian and circannual I Receptors•• cAMP changes are superimposed on these as are the demands of :.. ~cGMP reproduction. This review draws on examples of each, includ­ ""': 1---- IP, ing previously unpublished work, and attempts to delineate TARGET TISSUEc'------' __ some of the required but as yet wanting infonnation. Physiological Response Neuroendocrine regulation _-=-_======~_---'-J There is a large body of infonnation available on the neuroen­ .

) docrine pathways of physiological regulation in crustaceans. Figure 1 Sensory input from either internal or external receptors is 9

0 One of the more developed knowledge bases exists for the integrated within the eNS. Primary messengers (monoamines and 0

2 cardiorespiratory system, including heart function [whole peptides) are released from the pericardial organs (POs) and stoma­ d heaM (McGaw, Wilkens, McMahon & Airriess 1995; e togastric ganglion (STG) complex into the haemolymph. The sinus t

a Wilkens, Kuramoto & McMahon 1996), cardiac ganglion gland similarly releases peptide hormones, either under control of d

( (8erlind 1989; Cooke 1988), contractile propeMies (Wilkens the eNS or modulated by circulating neuroamines. Current hypothe­ r

e ef at. 1996], haemolymph redistribution mechanisms (Kura­ ses suggest that receptors associated with the y. and X-organs of the h s moto & Ebara 1984, 1989; Wilkens 1997)], aOMo-arterial i l eyestalk system are linked to cAMP 2nd messenger systems. A vari­ b valves (Wilkens, Davidson & Cavey 1997), venous valves

u ety of target tissues including the heart, arterial valves, ventilatory

P (Taylor & Taylor 1986), respiratory gas uptake and transpoM

muscles, branchial ATPases, locomotory muscles, fuel stores and the e in the haemolymph (Morris 1991). Much of this work has h haemocyanin are either affected directly or possibly via local nerv­ t been done on relatively well-defined models, although there y ous receptors and transmission. b

is often a gap between investigations of different levels of d

e control since various laboratory groups historically and inevi­

t impoMant physiological signals. In addition, the concept that n tably specialise in different preparations and species. There

a respiratory gases functi"on as signals controlling and integrat­ r has been a strong tendency to assume that mechanisms func­ g ing metabolism and physiological responses in crustaceans is

e tioning in one species or subgroup will also be present in c examined in some detail. n other less-studied species and while not necessarily wrong, e Contemporary repoMs, taken collectively, suggest that a c i such generalisations should be treated with caution since pro­ l

relatively small suite of messengers regulates and integrates a r nounced species-specific responses to neurohonnone signals e wide variety of physiological processes. The paramount ques­ d do occur. n tion is, how can this be? How do crustaceans generate spe­ u

Arguably one of the best studied and 'classical' endocrine y cific responses to the same, widely dispersed messenger

a control systems in the Crustacea involves the eyestalk sinus w molecules in separate systems? How are these systems modu­ glands (Figure I). These glands release a variety of peptide e t lated to respond variably but in conceM? For example, groups a honnones such as crustacean hyperglycaemic honnone

G of modified nerve tenninals in crustaceans, including the (CHH), gonad inhibiting honnone, moult inhibiting honnone t e pericardia I organs, release biogenic amines and peptides, and and red pigment concentrating honnone (Keller 1992) which n i the stomatogastric nervous system, can -respond to these same are primarily concerned with growth and reproduction. CHH b a biogenic amines. Other neurohaemal structures, in the eye­

S is thought to be the chief regulator of metabolic fuel availabil­

y stalk for example, are suggested to be responsive to neuroam­ ity in crustaceans,' and the release of this peptide from the b sinus glands is apparently modulated by the biogenic d ines and to release complexes of peptide honnones. Despite e c u d o r p e R S. Afr. 1. Zoo\. 1998, 33(2) 89

monoamines (LUschen, Willig & Jaros 1993; Kuo, Hsu & Lin A 1995; Sarojini, Nagabhushanam & Fingerman 1995). The Stimulation numerous peptide modulators of reproductive state will not Haemolymph be considered in detail here although a strong integrating ..::o,,--,--=~Po, & amines influence of these compounds seems likely, for example in Stomatogastric the context of the seasonal nature of locomotory energetics of STG Ventricular reproductive migrations. cAMP mediation & neurite transpor Neurohormones, amine- and peptide-signalling molecules r-----.::,~ released into the haemolymph from neurosecretory neurons, are stored in and released from, for example, the pericardial organs (PO). Substances released from the POs include Monoamine nerves 5-hydroxytryptamine (5-HT), octopamine (OA), dopamine release (DA), proctolin (PR), crustacean cardioactive peptide (CCAP) and several FMRF-amide related peptides (Beltz & Specific units fire in Kravitz 1986; Keller 1992). The POs consist of numerous modulated bursts in response neurosecretory terminals formed from the peripheral ramifi­ LP burst duration to SN stimulation cations and anastomoses of the second dorsal roots (segmen­ increases at low Po, & SN monoamine release tal nerves) of the thoracic ganglion (Alexandrowicz 1953) and can be stimulated both electrically and pharmacologically B Homarus gammarus C Panulirus interruptus to release their products (Cooke & Sullivan 1982). The POs are situated on the inner, lateral walls of the pericardial sinus, RecQrding from lateral Recordings fron lateral ventricular pyloric nerve nerve of the stomatogastric ganglion spanning the openings of the branchiopericardial veins and thus bathed by venous haemolymph returning to the heart. Their capacity to produce and store cardioactive amines and peptides means the POs of decapod crustaceans are well suited for a role in neurohumoural coordination ofphysiolog­ ical function (Figure I). Included in this capacity for physio­ logical coordination is the possibility that amine or peptide neurohormones released from the POs, acting through recep­ tors in the central nervous system (below), might provide Control Dopamine mr . ) feedback regulation of tonic levels of their own circulating 9

0 Figure 2 (A) The stomatogastric ganglion (STG) of crustaceans

0 concentrations. 2 The stomatogastric ganglion (STG) responds to monoam­ receives electrical input from the stomatogastric nerve, which also d e releases biogenic monoamines. Dopamine and 5·HT elicit increased t ines as well as electrical stimulation, resulting in intracellular a cAMP levels in different cells of the STG. Elevated cAMP causes d cAMP production and transport in the neurites of the STG, ( intracellular transport of cAMP within affected neurites. (8) r and ultimately electrical activity in the ventral nerves (Figure e Monoamine stimulation of the STG promotes increased electrical h 2; Hempel, Vincent, Adams, Tsien & Selverston 1996). The s i l nerves of the STG are associated with the oesophageal gan­ activity in at least two different units of the ventricular nerves. b u glia (Massabuau & Meyrand 1996), again illustrating the tight Located within the arterial lumen the STG will be sensitive to circu­ P

lating monoamines released remotely from the stomatogastric nerv­

e coupling of the CNS and neuroendocrine regulatory path­ h ous system (after Massabuau & Meyrand 1996). (C) Reducing the t ways. The location of the STG in the lumen of the anterior

y aorta means it will receive circulating honnones from the POs P02 of the haemolymph bathing the STG also promotes changes in b bursting patterns, but of specific cells of the lateral pyloric nerve. d and sinus glands (Christie, Skiebe & Marder 1995). Thus e t there is a demonstrated capacity for various parts of the nerv­ Thus the SrG is sensitive to haemolymph-bome monoamines, input n a ous system to communicate via haemolymph-borne messen­ from the nervous system and to internal hypoxia, and responds by r g gers and feed back into specific fibres and the CNS. For much specific motor directed outputs and likely feed· back to the eNS e c of our discussion, the origin of these substances is of little (after Hempel €I 01. 1996). n e

c importance but the fact that they are released into the haemo­ i l lymph from some neurohaemal organ in response to input r neurohormonal modulators into the haemolymph include e from the CNS, whence they can be transported to distal target d environmental hypoxia, the functional (internal) hypoxia n tissues and organs, is of crucial consideration. Equally impor­ u

associated with exercise or exposure to the inappropriate res­ y tant, the crustacean open circulatory system allows neurohor­ a mones released into the haemolymph to be brought into piratory medium (e.g. air exposure of water breathers), w e changing energetic requirements, disturbance to water bal­ t proximity with all tissues in the animal. This allows organ­ a ism-wide coordination of physiological function, but also ance/ion-homeostasis and changes in temperature. G t suggests the existence of mechanisms at the tissue and cellu­ Sites of action of the monoamine and peptide neurohor­ e n i lar level capable of modifying local responses to circulating mones are numerous. They include the myocardium, cardiac b

a neurohormones (if one assumes a general response is to be ganglion, cardioarterial valves, aorto-arterial valves, haemo­ S avoided in most instances). cyan in, scaphognathites, sinus glands, glucose storage sites in y b The types of challenge that might bring about a release of muscle and other organs, stomatogastric ganglion, branchial d e c u d o r p e R 90 S. Afr. J. Zool. 1998,33(2)

ion pumps and reproductive organs to list a few. Obviously Gleeson & Derby 1995). Although DA has obvious excitatory there must be neurohormone receptors in each of these target effects on the function of the stomatogastric system (Lingle tissues and organs, although these are not yet well known in 1981; Harris-Warrick, Coniglio, Barazangi, Guckenheimer & crustaceans, the impermeant nature of the neurohonnones Gueron 1995), it appears to have less striking and more dealt with here requires membrane-bound receptors as inter­ ambiguous influences on the cardiovascular system at likely mediaries to the subsequent activation of intracellular signal­ physiological concentrations. There are indications that DA ling pathways. There is a great deal of published work on exerts its excitatory effects on branchial Na'IK'-ATPase via receptor types, localisation and second messenger activation changes in intracellular cAMP levels (Morris & Edwards, in insects, and receptors for many of the same signalling mol­ 1995; see below), and that increases in stomatogastric gan­ ecules (particularly the amines) also exist in vertebrates. glion activity are brought about by DA-mediated decreases in Comparable work on receptor classification has yet to be car­ membrane K' permeability (Harris-Warrick et al. 1995). ried out on crustaceans. Synthesis of OA and DA from tyrosine occurs in separate Of the biogenic amines stored in crustacean POs, the indol­ cell types (Barker et al. 1972). Experimental release of OA amine 5-HT and the phenolamine OA are known to be from the POs can be induced by either electrical stimulation released in suffcient quantity in vivo to trigger cardiovascular (Sullivan, Friend & Barker 1977) or incubation in very high responses in some decapods (Florey & Rathmayer 1978; Sul­ K' (Evans, Kravitz & Talamo 1976) and is strongly livan 1978; Livingstone, Schaeffer & Kravitz 1981). The cat­ Ca"-dependent (Sullivan et al. 1977). Much more is known echolamine DA is also found at a high concentration in the about the actions of OA as an invertebrate neurohonnone POs of several crab species (Cooke & Goldstone 1970). All than about the equivalent roles of 5-HT or DA, owing in part three of the pericardial monoamines possess excitatory prop­ to its ubiquity in arthropod neuromuscular systems (Nathan­ erties in studies of isolated decapod hearts (Beltz & Kravitz son & Greengard 1973, Florey & Rathmayer 1978; Benson 1986; Wilkens et al. 1996), but each has markedly different 1984; Morton 1984; Rane, Gerlach & Wyse 1984; Whim & effects, for example, on the electrical activity of the stomato­ Evans 1988; O'Gara & Drewes 1990). In the isolated CG of gastric ganglion (Hempel et al. 1996). Neurogenic peptides the crab Portunus sanguinolentus, OA caused a decrease in are also released from the POs and can have different excita­ burst frequency together but with increased burst duration at tory effects, for example, on the cardiac ganglion (Lemos & concentrations up to I )lmol.l-' (Benson 1984). At higher con­ Berlind 1981). The peptides proctolin, FI and F2 markedly centrations (5-10 )lmol.l-') this inhibition of burst frequency influence heart rate and stroke volume in decapods (McGaw was overshadowed by excitation of the CG and higher than et al. 1995). control rates of bursting in some cases. The action of OA on

. Many of the actions of 5-HT on cardiovascular targets in the CG of crabs is thought to be a result of inhibition of the )

9 decapods are likely to be brought about via a cyclic AMP motor neurones since bursting continues unabated in the 0

0 (cAMP) mediated second messenger system (Battelle & pacemaker cells. In the lobster P. japonicus, the burst fre­ 2

d Kravitz 1978; Lemos & Berlind 1981). Lemos & Berlind quency of the CG pacemaker cells is inhibited by OA under e t (1981) concluded that the involvement of cAMP in the car­ conditions of minimal myocardial stretching (Kuramoto & a d Ebara 1991) but at high internal pressures it caused an ( diac ganglion (CG) response to 5-HT is probably much lower

r increase in burst frequency. Elevated cAMP levels occurred e than in the myocardium, since the increase in cAMP in the h s CG was smaller. Experiments investigating the effects of in the myocardium of both crab and lobster in response to OA i l

b cAMP on ion transport have suggested that this intracellular treatment (Sullivan & Barker 1975; Battelle & Kravitz 1978). u messenger is also involved in stimulation of Na'-uptake by P Proctolin, a pentapeptide hormone found in the pericardial e the gills of Callinectes sapidus (Lohrmann & Kamemoto, organs and in the sinus glands, as well as within the input of h t 1987). the stomatogastric ganglion (Keller 1992; Christie et al. y b

Cooke & Goldstone (1970) demonstrated that 5-HT and 1995) has excitatory effects on isolated crustacean hearts, d e DA are sequestered in separate nerve terminals within the increasing both the rate and force of contraction (McGaw et t n POs ofbrachyuran crabs. DA is produced in cells of the POs al. 1995; Wilkens et al. 1996). However, proctolin is cardio­ a r

g from its precursors, L-dihydroxyphenylalanine (L-DOPA) inhibitory when applied to intact animals (McGaw, Airriess

e & & McMahon 1994a; McGaw et al. 1995), supporting the sug­ c and tyrosine (Barker, Molinoff Kravitz 1972) but is stored n gestion of modulation of peptide hormone effects by the CNS e in smaller quantities than 5-HT (25-33%) in the POs of both c i l Panulirus (Sullivan, Friend & McCaman 1976) and Carcinus or other circulating neurohonnones, Proctolin has pro­ r

e (Cooke & Sullivan 1982). DA acts primarily on the small nounced effects on the cardioarterial valves of decapods, d pacemaker cells of the crab (Portunus sanguinolentus and causing strong rhythmic contraction of the sternal valve n u

PodophJhalmus vigil; Miller, Benson & Berlind 1984). The (Kuramoto & Ebara 1989; Kuramoto, Wilkens & McMahon y a threshold for DA effects on the isolated CG is approximately 1995). When applied subsequent to red pigment concentrat­ w

e 10 nmol.l I and, interestingly, at near-threshold concentra­ ing hormone to the stomatogastric nervous system of the lob­ t a tions, CG burst duration tends to increase in conjunction with ster Panulirus interruptus, proctolin activates the cardiac sac G &

t a decrease in burst frequency. DA has been shown to increase motor pattern (Dickinson, Fairfield, Hetling Hauptman e

n intracellular cAMP levels (Hempel et al. 1996) and also to 1997) but has no effect when applied alone in this prepara­ i b enhance neuromuscular communication by either pre- or tion. Reproductive and swimming behaviours appear to be a S

post-synaptic mechanisms (Lingle 1981). A role in modifica­ altered by proctolin in C. sapidus (Wood 1995). The mode of y

b tion of the courtship behaviour of Callinectes sapidus is also action of proctolin at target cells is not known in crustaceans,

d suggested for DA, in conjunction with proctolin (Wood, but in insects the peptide is thought to elevate intracellular e c u d o r p e R S. Afr. J. Zool. 1998, 33(2) 91

(Ca'+) via the production of inositol 1,4,5-triphosphate (JP,) the supraoesophageal ganglion. The paired anterolateral arter­ and inositol 1,3,4,5-tetrakisphosphate (JP,) (Hinton & ies arise lateral to the anterior aorta and supply haemolymph Osborne 1996). to the testes, digestive gland, integument and antennae. The physiological responses of crustaceans to experimental Haemolymph delivered via branches of these vessels also infusion of the pericardial monoaminos implies considerable perfuses the supraoesophageal ganglion, the optic ganglia and complexity in the interaction of various control systems. With the oculomotor muscles (Baumann 1921; Sandeman 1967). potential targets in the CNS, in the various neurohaemal The hepatic arteries, too, are paired vessels originating organs and in distributed effector systems, the modulation of slightly medial and ventral to the anterolateral arteries and neurohormone activity by other neuromodulators is probable, delivering haemolymph to the gut and digestive gland. The and results in a multi-tiered system with potential feedback sternal artery is a large non-paired vessel arising at the ventral regulation at several possible levels of control. In addition, it side of the heart. This vessel runs anteroventrally before seems very likely that most effects of neurohormones are branching to form the ventral thoracic artery which supplies modulated or overridden by neural regulatory mechanisms in haemolymph to the cephalic appendages, the anterior portion whole animals, such that responses in vivo are quite different of the ventral nerve cord and the digestive gland; and the ven­ to those recorded in vilro. The most effective dosages of tral abdominal artery, which delivers haemolymph to the pos­ monoamines utilised experimentally are probably much terior region of the ventral nerve cord and the ventral side of higher than those required for activity under natural condi­ the abdominal musculature. The thoracic ganglion of the CNS tions. Lower circulating levels of effector substances would is perfused with haemolymph from branches of the pedal allow finer adjustment of physiological performance to meet arteries. These vessels arise from the ventral thoracic and specific metabolic requirements, but such fine adjustments ventral abdominal arteries and also deliver haemolymph to may not be detectable in investigations which rely on the the pereiopods. The median posterior aorta originates in close analysis of grouped data from many individuals. proximity to the sternal artery, and supplies haemolymph to the musculature of the abdomen and pereiopods. Oxygen demand, availability and delivery Until recently, the absence of vasoconstrictive musculature The cardiovascular system is responsible for the conduction in the walls of decapod crustacean arteries was considered of haemolymph and the transport of 0" thus the optimisation indisputable (Maynard 1960; Shadwick, Pollock & Stricker of the circulatory system is important in maximising 0, deliv­ 1990): Striated muscle has now been described, however, in ery for minimum cost. The multitude of effects of the pericar­ the posterior aorta of the prawn Sicyonia ingentis and the lob­ dial neurohormones on the decapod crustacean heart, taken ster Homarus americanus (Martin, Hose & Corzine 1989; together with the proximity of the pericardial organs and Wilkens el al. 1997). In H. american us vascular resistance to . ) haemolymph flow can be modulated by a variety of neuro­ 9 heart, strongly suggest an important role in cardiovascular 0

0 regulation and respiratory gas transport for the POs. In addi­ transmitters and neurohormones (Figure 3; Wilkens 1997) 2 tion, the concentrations of neurohormones released from the and in the abdominal aorta these changes in resistance are d e

t POs must be highest at the heart, before dilution in the circu­ thought to be brought about by valves at the origin of lateral a lating haemolymph has occurred. Electrical stimulation of the d (

r segmental nerves of Panulirus interruptus brings about the A B J AnteriQr median artery e [; Dorsal abdominal artery h sudden, quantal release of enough pericardial 5-HT to elevate 60 Segmental lateral s 200 • Sternal anel)' i 1 arteries Qpen l the circulating concentration of this amine to 1.2 nmol.l- b u (Sullivan 1978); the concentration of 5-HT at cardiac targets ~150 P must be many fold higher. e ~ 100 h t The regulation of heart beat frequency and cardiac stroke

E y volume by the Crustacea is dependent on the unique innerva­ .;;; 50 b ~ 25 d tion of the neurogenic crustacean heart. The cardiac ganglion e .- 10 t (CG), consisting of nine neurones arranged in a characteristic " n a pattern on the inner dorsal wall of the heart (Alexandrowicz 5 r ~ g 1932), generates rhythmic burst discharges which induce e e c myocardial contraction. In addition to nervous regulation via o n e

c synaptic input from the cardioaccelerator and cardioinhibitor i l nerves, which arise from the central nervous system, the fre­ r e quency of CG bursting appears to be altered by neurohormo­ d n nal agents (Guirguis & Wilkens 1995). Figure 3 Effects of pericardia I neurohormones on arterial resistance u

y In decapod crustaceans, seven major systems of arteries to hacmolymph flow in the lobster Homarus americanus (after a originate at or near the heart and supply haemolymph to dis­ Wilkens 1997). (A).Increased resistance to flow through the abdomi­ w e t tinct body regions and organs (Pearson 1908). The exact ori­ nal aorta with the segmental arteries open in response to 5-HT and a gin of each artery is variable among sub-groups, but the same proctolin. (8) Relative increases in resistance to haemolymph flow G

t through v.esscls supplying diverse regions in response to biogenic

e seven vessels occur in all species and deliver haemolymph to n i the same morphological regions (Miller 1895; Pearson 1908; amines and peptidcs. These changes in resistance occurred b down-stream from the heart and cardioarterial valves, suggesting a Baumann 1921; Belman 1975). The anterior aorta is a median S dorsal vessel which supplies haemolymph to the eyestalks other active mechanisms to control the redistribution of haemo­ y b

and their associated sinus glands, and to the antennules and lymph pumped by the heart. d e c u d o r p e R 92 S. Afr. J. Zoo!. 1998,33(2)

arterial branches. Work on Homarus and Panulirus has A shown muscular, innervated semilunar valves are present at 25 _ PR(IOnmol·r') the origin from the heart of each of the anterior arteries; the ~ OA (I ~mol·r') sternal artery and posterior aorta share a common valve in ~ 20 0[) Panulirus japonicus Panulirus (Alexandrowicz 1932; Kuramoto & Ebara 1989; E Kuramoto, Hirose & Tani 1992). Each of the valves receives ~ 15 innervation via fibres originating from the CNS (Alexandro­ .8'" wicz 1932), and can contract, in isopods, in response to neural Ii'" 10 (Kihara & Kuwasawa 1984; Kihara, Kuwasawa & Yazawa E-

) lower than those employed in experimental manipulations

9 dioarterial valves. Proctolin also increases tension in the anterior 0 might be more effective when released from the pericardial 0 valve muscle while octopamine has no effect (after Kuramoto & 2 organs under natural conditions owing to the close proximity Ebara 1984). (B) Haemolymph flow through the anterolateral arter­ d e of target receptors in the cardiac ganglion and myocardium. t ies of Cancer magister is decreased slightly following proctolin a At the cardioarterial valves, 5-HT causes hyperpolarisation d infusion but is increased by octopamine. Both neurohormones ( of all valve muscles, leading to relaxation of the valves and r increase flow through the sternal artery (after Airriess 1994 & e

h unimpeded haemolymph flow. OA relaxes the muscle of the McGaw et al. 1994a). s i l anterior cardioarterial valves whilst causing the muscle of the b

u posterior valve to contract (Figure 4a; Kuramoto & Ebara P 1984), so is potentially capable of redirecting haemolymph of apnoea and cardiac arrest which have been described for e h flow toward cephalic structures in intact animals. DA hyper­ t decapods resting in well-aerated seawater (Burnett & Bridges

y polarises the posterior cardioarterial valve muscle in H. arner­ 1981). Cyclic patterns of arterial and venous perfusion are b icanus (Kuramoto el at. 1992), allowing maximum haemo­ d seen in the terrestrial brachyuran Gecarcoidea natalis, and e t lymph flow through the sternal artery and posterior aorta. changes in these patterns are observed following treatment n a Proctolin causes depolarization and contraction of all of the with pericardial monoamines (Figure 5). Such cyclic changes r g

cardioarterial valves (Figure 4a) and also induces rhythmic and diversions in flow suggest sensors and control systems e c contractions of the posterior valve (Kuramoto & Ebara 1984, responding to thresholds in 0, availability. The reconfigura­ n e 1989) although the latter effect can be overcome by inhibitory tion of pattern generators in the stomatogastric ganglion by c i l

nerve stimulation (Kuramoto el at. 1995). Apparently contra­ neurohormones and oxygen (Hempel el al. 1996; Massabuau r e dictory effects on arterial haemolymph flow in vivo and in & Meyrand 1996; Figure 2b) provides one mechanism by d n different species (Figure 4b) as well as down-stream modula­ which peripheral and haemolymph 0, changes can be trans­ u tion of arterial resistance (Wilkens 1997) clearly indicate that duced to changes in perfusion. y a the physiological role of the cardioarterial valves and other In responding to environmental hypoxia, it is crucial that w e mechanisms of haemolymph redistribution need considerable t uptake of 0, from the ventilatory medium be maintained a further investigation. without compromising off-loading at the tissues. General G t The spontaneous alternation of haemolymph delivery via responses to hypoxic exposure are well known in Crustacea, e n i the sternal artery and anterolateral arteries of control animals and much work has been devoted to understanding the ability b

a which occurs between brief periods of cardiac arrest of aquatic decapod crustaceans to maintain respiratory func­ S (McGaw, Airriess & McMahon 1994b) may be an energy­ tion independent of environmental 0 1 partial pressure above y b

saving mechanism supplementary to the well-defined periods certain, species-dependent, critical levels. As a result of the d e c u d o r p e R s. Afr. J. Zool. 1998,33(2) 93

~ an increase in cardiac stroke volume, allowing cardiac output ""i"c 140 Heart rate to be maintai ned at near-nonnal levels during acute hypoxic .§ 120 exposure (Airriess & McMahon 1994; Reiber 1995). ~ G 100 Increased perfusion of the sternal artery of crabs (Airness & c McMahon 1994) and crayfish (Reiber, McMahon & Burg­ g 80 L _~ ___ gren 1992) augments the supply of haem olymph to the if.... scaphognathites, su pporting a 50-200% in crease in pumping '" frequency (Figure 6a). Below the critical partial pressure of 4 0, (Pc) the work of the scaph ognathites and heart requires Antenor aorta more energy than can be harnessed using aerobic metabolism; 3 M02 can no longer be maintained and the venous O 2 reserve 2 is depleted. Anaerobic metabolism may take over in so me 1 '!>1~UJII.%iI'IIIJ species although th e scope for this, as well as th e ability to maintain oxygen consumption despi te environmental O2 o~~==~~~~~~~ depletion, is highly variable among species (McMahon 1988). 60 There is some evidence of neurohonnona l respon ses to Pulmonary vein hypoxia. Of the neurohonnonal modulators with cardioactive 40 properties, proctolin is the most likely effector involved in th e 20 responses to hypoxia observed in crabs and crayfi sh. Increases in scaphognathite pumping rate have been reported O~~~~~~~~~~~~~~~ following administration of this peptide (Wilkens, Mercier & Evans 1985), as have concurrent bradycardia and increased 0.3 cardiac stroke volume in vivo (McGaw ef a/. I 994a; 1995). 0.2 The shift of a greater proportion of haemolymph into the ster­ _Branc----+hial 0.1 :r_essure------.....,.~ nal artery of Cancer magister during hypoxic exposure is also ~ 0.0 '" -0.1 '"~ -0.2 A p... -0.3 LL..~~~~L....~...J.....~~~~""""~~ _ Anterolateral artery 140

. 10 20 30 40 60 7 ) 50 o Sternal artery 120 9 6 Ventilation rate 0 Time (min)

0 100 2 Figure 5 In Gecarcoidea nalalis pericardiaJ 5-HT infusion (I jJmol. 5 d 80 e I-I; arrow) causes an increase in heart beat frequency, branchial 4 t a chamber pressure and haemoJymph flow through the anterior aorta 60 d 3 ( and pUlmonary veins . Superimposed on the changes in haemolymph r 40 e 2

h flow are spontaneous fluctuations which become more pronounced s

i 20 l after 5-HT treatment. Note that flow through the anteri or aorta b declines after approximately 10 min whilst heart rate and flow u o o P

through the pulmonary vein remain elevated. HaemoJymph flow was Nonnoxic Hypoxic (3 kPa) e

h measured using a pulsed-Doppler flowmeter, heart beat frequency t B y was determ ined from the mean duration between systolic flow b peaks. d 10 e t n 8 a r g

much ·Iower 0 , solubility in water than air, water-breathing e 6 c species must ventilate their gas exchange organs at a hi gher n e rate than air breathers in order to maintain comparable arterial c 4 i l

O,levels (e.g. Morris 1990). Along with the greater viscosity r e of the respiratory medium , this presents special problems to 2 d

n aquatic crustaceans faced with environmental hypoxia which u must ·expend as much as 30% of resting oxygen consumption o y Saline 10 a for ventilation of the gills (Burggren & McMahon 1983; w e Wilkens, Wilkes & Evans 1984) and to these species match­ Treatment t a ing of gill ventilation and perfusion is critical. Figure 6 (A) Changes in ventilation rate and hae molymph fl ow G

t In general, gill ventilation increases as PO, declines below through the anterolateral and sternal arteries of Cancer magister as a e n result of dec reased environmental P0 (after Airrie~s & McMahon i nonnal environmental levels and oxygen consumption (MO,) 2 b is maintained although heart beat frequency may decline as 1994). (8) Haemolymph flow through the anterolateral and sternal a S 0, delivery to the myocardium is compromised (Wilkens arteries was similarl y affected by peri card iai infusion of proctolin y

b (after McGaw el af. 1994.).

1993). Along with a decrease in heart beat frequency there is d e c u d o r p e R 94 S. Afr. J. Zool. 1998,33(2)

seen following proctolin infusion (Figure 6b; Airriess & direct nervous stimulation by the cardioaccelerator nerves of McMahon 1994; McGaw e/ al. 1994a). Attempts to measure the CNS thus seems likely. circulating levels of neurohormones in crustaceans using It would be simplistic to believe that haemolymph distribu­ HPLC have met with limited success, owing to the minute tion and thus the transport of 0, and CO, is affected only in concentrations involved and problems in sample purification. times of 'stress' or extreme physiological challenge. A model The strong circumstantial evidence linking proctolin to the whereby respiratory gas transport is optimised by the effects physiological effects of hypoxia would be substantiated if of biogenic, cardiovascular-active amines and peptides is measurements of increased circulating concentration of this seductive to the crustacean physiologist. A finely graded sys­ peptide during hypoxia could be obtained. tem that can respond, in a sophisticated fashion, to minor The cardiorespiratory demands imposed by exercise are changes in respiratory requirements on a routine basis is similar. to those experienced during environmental hypoxia, clearly implicated. For example, the concept of 'sleeping' except that the availability of ambient 0, is not limiting. crustaceans suggests that large and significant changes in Therefore, as long as cardiac output can be increased to sup­ mechanisms supporting tissue 0, provision occur during the ply tissue 0, demand, internal, functional hypoxia does not transition between various resting conditions. Forgue el al. develop. Increased cardiac output must be brought about by (I992a,b) suggested that haemolymph 0, was typically very increased heart rate and/or stroke volume; in some cases there low only in truly quiescent animals, close to the threshold of may be an increase in both variables (Adamczewska & Mor­ anaerobiosis. The slightest disturbance stimulated the ventila­ ris 1994; DeWachter & McMahon 1996b). Along with tory and cardiovascular systems to raise haemolymph 0, lev­ increased perfusion of gas exchange structures, there is a cor­ els. Logically, this is acceptable since low PaO, maximises responding elevation of ventilation rate during exercise. the gradient for diffusion of 0, into the haemolymph and Increased haemolymph supply to the scaphognathites and minimises ventilatory costs. The magnitude of the cardiovas­ locomotory appendages via the sternal artery is therefore cular response will depend on, and be integrated with, haemo­ required, and has been demonstrated in two brachyuran spe­ cyanin 0, capacity. Important corroboratory data come from cies (DeWachter & McMahon 1996; McMahon, Airriess & the terrestrial Christmas Island red crab (G. nalalis) which Airriess 1996) along with a relative decrease in perfusion of utilises both lungs and gills for air breathing. This species is other arterial branches. Based on our knowledge of cardiores­ diurnally active and 'sleeps' at night. In the field, sleeping red piratory modulation it is probable that a single neurohormone crabs direct very little haemolymph through the pulmonary is not responsible for the diverse changes in cardiac function, pathway of venous return (Figure 7); but during the day scaphognathite beat frequency and arterial perfusion during awake, resting, crabs show much more equal perfusion of the pulmonary and branchial circuits. Thus, without any real res­

. exercise. As suggested for environmental hypoxia, proctolin )

9 could bring about an increase in scaphognathite frequency, piratory challenge large changes in patterns of perfusion 0

0 cardiac stroke volume and perfusion of the sternal artery; this, occur and must reflect altered priorities of the gills and lungs, 2 however, does not account for the massive increase in heart presumably to optimise oxygenation of the arterial haemo­ d e t rate which occurs during exercise (e.g. McMahon el al. lymph. Putative increases in circulating neuroamines might a

d 1996). The involvement of more than one neuromodulator, or modulate and integrate the various components of this ( r e h s *# i

l 75 b Sleeping crabs u

P Resting crabs •~ e -= h ~ 60 t

y .~.., b d

e = t 45 * ~ n -'" a .. ~ r • > haernolyrnph g -= e c:>. # Gill> Lung c 0 30 n '" e .. c

'. r ::; e 15 d ~ n = u y a 0 w e t Haemolymph Lungs Gills a G

t Tissue/Organ e n i Figure 7 Christmas Island red crabs, Gecarcoidea natalis, were injected in the field with 57CO labeled microspheres (15J.1m; as per Taylor & b a Greenaway 1984). Sleeping crabs were injected between 4.15 and 4.30 am, 2 h prior to sunrise; the resting crabs at least 3 h after sunrise. The S

y microspheres were allowed to circulate and lodge for at least 20 min after injection (Airriess, CN. & Morris, S., in prep.). Major changes in b the relative perfusion of gills and lungs are obvious when comparing these two quiescent states. d e c u d o r p e R S. Afr. J. Zool. 1998,33(2) 95

response but there have been insufficient attempts to resolve impulses in the stomatogastric nervous system (Figure 2b). this, compounded by the very real difficulties in measuring That 0, and CO, also act as signals and modulators of res­ the very small changes in modulator concentrations likely to piratory status, prompting responses that optimise their trans­ be involved. port, is an important concept. The regulation of haemocyanin It seems axiomatic that crustaceans must be provided with transport of 0, and CO, is now understood to be as complex receptors to control the drive of ventilation and perfusion. as that of vertebrate haemoglobins. Oxygen transport must be Ventilation is primarily 0, driven in water breathers but there optimised for both loading and unloading, and most fre­ is some evidence to suggest that CO, acts as a ventilatory quently has been assessed in crustaceans with respect to stimulus in air-breathing decapods (McMahon & Burggren either environmental hypoxia or exercise (Morris 1990, 1991; 1988; Morris 1991 for reviews). Some evidence points to Burnett 1992; Truchot 1992; Morris & Bridges 1994 for internal receptors closely associated with the CNS (e.g. reviews). The ventilatory and cardiovascular adjustments to Wilkens, Young & DiCaprio 1989). However, oxygen sensi­ hypoxia (above) serve to match 0, delivery to demand (i.e. tive receptors were described by Ishii, Ishii, Massabuau & maintain O2 constant as a signal) but the reciprocal changes in Dejours (1989) in the branchiopericardial veins of crayfish CO, markedly influence haemocyanin function and thereby

suggesting peripheral O 2 sensors drive ventilation, as corrob­ O2 delivery. This is possible since in nonnal aerobic metabo­ orated by Zinebi, Simmers & Truchot (1990) for Carcinus lism 0, and CO, are linked by respiration and in their trans­ maenas. While Reiber (1997a) makes a similar conclusion, port (Bridges & Morris 1989, review). Thus a hyperventi­

suggesting that branchial O2 receptors influence cardiovascu­ latory response to environmental hypoxia promotes CO, lar responses to hypoxia, he suggests that ventilation responds excretion and haemolymph alkalosis, leading to an adaptive to more centrally situated receptors. These drives provide the increase in oxygen affinity. Since metabolic demand is not proximal stimulus for neurohormone release and thereby the otherwise greatly increased the primary effect is to facilitate coordinated response in ventilation, cardiac function and per­ loading from an 02-poor environment.

fusion patterns. Recent pivotal work by Massabuau & In contrast, during the initial phases of exercise, O2 demand Meyrand (1996) implicates centrally mediated drivers and is increased and CO, production elevated promoting a hyper­ has provided direct evidence of the transduction of haemo­ capnic acidosis, reduced haemolymph pH and thereby a low­ lymph PO, into nervous input to the CNS. Lowering PaD, to ered Hc-O, affinity (Figure 8). However, in these circumstan­ 2 kPa in lobsters (Homarus gammarus), just above the anaer­ ces the environment is most frequently well oxygenated and obic threshold, significantly increased the duration of burst arterial saturation maintained by hyperventilation; thus, the . )

9 P. warreni - Effect of exercise - curves at in vivo pH 0 0 2

d ER e t f::: .- a 5 d ~ (

N 0.8 r e Q. h ;> s

i o l

P Exercised A: e h t

y 0.4

b Decrease in P 0 & greater a-v diff

v 2

d S ifinadequate compensatory e t increase in Qh n 0.2 a r g

Hyperventilation effect e c ~ n

e 0 c i l P0 (kPa) 2 r P,O, (R) P,O, (E) e d PP,(R) P,O, (E) n u (E,)

y pp, a w Figure 8 Model for integration of ventilation, perfusion and haemocyanin oxygen affinity during aerobic exercise. Resting (R) Pa0 2 and Pv0 2 e t lie on the equilibrium curve such that -25% of bound O is released to the tissues. A respiratory acidosis induces a Bohr shift and reduces a 02 2

G ) Hc-02 affinity. The hyperventilatory response to exercise sustains O2 loading (P• .o 2 and provides for a higher Pv0 2 (E) and assists in 02 dif­ t e fusion into the tissues. The a-v [021 difference can be maintained similar to that in resting animals providing cardiac output is increased pro­ n i portionally. Increased or sustained exercise, or a failure of perfusion, must lead to increased a-v [0 1difference and thus a decrease in Pv02

b 2 a (E2)' Therefore. while hyperventilation is integrated with Hc-02 affinity to maintain loading, the Pv 0 must be integrated with and dependent

S 2

y on the capacity to increase haemolymph flow and redirect perfusion. Curves for resting and exercised Potamanautes warreni (Adamczewska, b van Aardt & Morris 1997). d e c u d o r p e R 96 S. Afr. 1. Zoo I. 1998, 33(2)

limitations on 0, supply are primarily at the site of unloading, and facilitated by the lowered 0, affinity. While this decrease 0.10 ... ~... • Control in Hc-O, can assist 0, diffusion into the tissues by raising the ...... o Chilled P vO" the diffusion gradient and protection of the 0, venous 0.08 ...... Non-chilled • reserve depend on the extent to which cardiac output can be increased and perfusion patterns optimised. Logically, there must be central 0, receptors (above), or perhaps CO, recep­ tors in air·breathers, that sense respiratory status and initiate the necessary cardiovascular and ventilatory compensations, via neurohormone release, matching these to the 0, and CO, transport characteristics of the haemocyanin. In addition to promoting and co-ordinating mechanical 2 4 6 8 10 12 14 16 18 adjustments of the cardiorespiratory system, haemolyrnph­ borne neurohormones are very likely to influence the function of crustacean haemocyanins (Morris 1990, 1991; Morris & 1.0 Bridges 1994; for reviews). Some monoamines, especially dopamine, act directly on haemocyanin to increase oxygen 0.8 affinity (Morris & McMahon 1989) and thus provide a recip­ rocal signal, whereby the Hc-O, affinity can potentially be 0.6 fine tuned for closer integration with ventilation and circula­ tion. There is some suggestion, however, that monoamine 0.4 binding by haemocyanin may be an indication of transport! [ur.te] 3.52 mmol.L", 20"C enzymatic function of the protein (Morris & McMahon 0.2 1989). The bases of integration between cardiovascular func­ [urate] 0.02 mmol.L", 20"C tion, haemocyanin function and respiration requires careful investigation under realistic ecophysiological circumstances. o 2 4 6 8 As the duration and extent of respiratory challenge P.o2 (kPa) increase, either ventilatory compensation or more likely hae­ molymph perfusion will fail to maintain 0, delivery at the Figure 9 Circulating [urate] increases when Pa02 falls below that required to support urate oxidase activity. Top panel shows effect of

. required rate. Lowered P,O, and especially low PvO, are ) hypoxia on haemolymph urate in southern rock lobsters, .Jasus 9 clear indications that the feedback between 0, as a signal and 0 edwardsii. Control animals were held in normoxic water at 18°C and 0 0, supply has exceeded the capacity of mechanical and bio­ 2 chemical compensations. Decapod crustaceans, at least, pos­ hypoxia was induced by air exposure at both 18°C (non-chilled) and d

e 5°C (chilled). Note that chilling ameliorates the increase in urate at t sess a further suite of effectors that operate under these a the same PaOzo The lower panel shows O2 equilibrium curves from d circumstances. (

Jasus edwardsii haemolymph at high and low temperature, demon­ r Urate has been identified as modulator of Hc-O, binding, e strating the direct effect of temperature on Hc-02 affinity. In .Jasus, h increasing the affinity for 0, (Morris, Bridges & Grieshaber s i urate also markedly improves the O2 affinity ofthe Hc (Morris, S. & l 1985, 1986; Lallier, Boitel &' Truchot 1987; Nies, Zeis, b Olliver, S., in prep.). u Bridges & Grieshaber 1992; Zeis, Nies, Bridges & Gries­ P

e haber 1992). Urate is an intermediate in the purinolytic path­ h t way to urea and NH" and is oxidised by urate oxidase (UO) is simultaneously impaired. However, in many crustaceans y

b requiring 0, as co-substrate. When circulating and tissue 0,

that routinely experience hypoxia, L-Iactate has a specific d decline, especially during hypoxia the rate of urate catabo­ e effect, partially opposing the reduction in affinity caused by t lism, depending on the affinity of UO for 0" will slow and n lowered pH (Truchot 1980; Morris 1990; 1991). Thus, as the a r urate will accumulate (Figure 9; Dykens 1991). Thus under ventilatory and cardiovascular adjusttnents become progres­ g conditions in which the 0, signal is not so low as to promote e sively inadequate in matching 0, supply to demand, specific c anaerobiosis, there is a progressive increase in urate concen­ n mechanisms to sustain 0, transport become important. L-Iac­ e c tration, a consequent improvement Hc-O, affinity and thus in i tate has most pronounced effects during the crucial, initial l 0, loading, providing some support for maintaining 0, sup­ r stages of the recruittnent of anaerobiosis into energy metabo­ e d ply. Changes in tissue urate occur relatively slowly and seem lism, reducing further 'right-shift' of the Hc-O, equilibrium n more important in the long term than during episodic exer­ u curve and thereby assisting to some extent the hyperventila­

y cise. tory response in support of 0, uptake. a

w Rapid or sustained exercise often increases O2 demand Of some interest is the recent suggestion that both e t beyond the capacity of the delivery system. Haemolymph 0, monoamines and L-Iactate may be important in inducing and a

G then quickly declines and anaerobiosis is initiated. L-Iactate is regulating behavioural hypothermia in decapods (De Wachter, t e the end product of anaerobiosis in crustaceans, and a progres­ Sartoris & Portner 1997). This is an intriguing response n i sive lactacidosis results from 0, shortfall. While the concom­ whereby hypoxia encourages animals to seek out lower ambi­ b a itant acid production will reduce Hc-O, affinity and facilitate ent temperatures, lowering the metabolic rate and therefore S

y 0, unloading, this is of little utility under extreme hypoxia, 0, demand and maintaining high internal 0, levels. This b functional or environmental, if 0, loading at the gills or lungs behavioural response might well enable crustaceans to avoid d e c u d o r p e R S. Afr. J. Zool. 1998, 33(2) 97

a number of costly compensatory responses (see below). CHH (Keller, Jaros & Kegel 1985), although mRNA encod­ Aquatic crustaceans transferred into air suffer extreme ing two CHH isoforms have been localised in other regions of functional hypercapnic hypoxia, largely owing to the failure the CNS (de Kleijn, Leeuw, van den Berg, Martens & van of the gills in respiratory gas exchange. Conversely, species Herp 1995). The amino acid sequence of CHH is highly adapted to life on land frequently drown in water. In both of homologous with moult-inhibiting hormone (MIH), another these groups exposure to the alien environment results in a product of the sinus gland in crustaceans, and high affinity rapid switch to anaerobiosis. However, some crustaceans reg­ binding sites for CHH are found in the V-organ (Webster ularly move between air and water, with some ability to 1993) indicating possible involvement in the control of breathe both media. Air-breathing crabs have lungs but retain moulting and reproduction. The mechanism of action of CHH gills for ion regulation and nitrogen excretion (see below). is not well established but available evidence suggests that it Taylor & Greenaway (1984) showed that Hollhuisana trans­ stimulates a G-protein coupled receptor in the membrane of versa increased perfusion of the gills while in water and the target cells, leading to increases in intracellular cyclic nucle­ lungs during air-breathing. Similarly, the Christmas Island otides (Sedbneier 1987) and IP, (Smullen, David & Pitman blue crab, Cardisoma hirtipes, exhibits quite different per­ 1996) and promoting increased intracellular glucose levels. It fusion of the gills and lungs while in air compared to when has been demonstrated that the digestive gland, abdominal breathing water (Airriess, C.N. & Morris, S., in prep). Evi­ musculature, gonads, gills, integument and haemolyrnph are dence from perfusion studies under other circumstances sug­ all targets for CHH (Keller & Andrew 1973; Santos & Ste­ gests that such changes in perfusion may be under active fanello 1991; Kummer & Keller 1993), but there is great spe­ control or be passive responses to alterations in venous resist· cies-specificity among the target tissues (Keller el al. 1985; ance. In the former case there must be a mechanism to sense Santos & Keller I 993a). the change in respiratory media and respond with a switch to CHH, and also the other amine and peptide products of the utilisation of the appropriate gas exchange organ. Changes sinus glands, are released into the haemolymph which is between air and water breathing would tend to promote large delivered to the optic ganglia via the optic and oculomotor respiratory acid-base changes. However, in truly amphibious arteries. These vessels arise as paired branches from the ante­ species, for example some grapsid crabs, these disturbances rior aorta and anterolateral arteries respectively (Baumann are transitory and minor (e.g. Morris, Greenaway & McMa­ 1921; Sandeman 1967), implying that preferential changes in hon 1996; Morris & Butler 1996) and thus CO, excretion can arterial perfusion, shifting haemolymph into or away from the be managed and integrated with the ventilatory and perfusion anterior dorsal arteries could affect the distribution - and adjustments for 0, uptake and delivery. Considerable further thus modulate the activity - of hormones from the sinus work is required to properly elucidate the interrelationships

. glands. Monoamines such as 5-HT and OA, which have ) between ventilatory and carC:iovascular adjustments, per­ 9 effects on cardiac output and the redistribution of haemol­ 0 fusion of twin gas exchange organs, and respiratory status and 0 ymph (see above), could therefore affect haemolymph glu­ 2 acid base balance in amphibious crustaceans as well as their cose concentration by altering the delivery of CHH as well as d e fully aquatic and terrestrial counterparts. t through direct effects on the sites of carbohydrate storage. a d Furthermore, there are strong suggestions that 5-HT, OA and (

r Energetics and Metabolism DA act on dedicated receptors at the sinus glands to alter hor­ e h mone release (Kuo el al. 1995; LUschen et al., 1993; Sarojini s Glucose is the major circulating carbohydrate in crustaceans i l el al. 1995) and thus modulate indirectly the concentration of b and levels of this energy source must be regulated in response u to metabolic status and requirements. Increases in circulating glucose in the haemolymph. P

e glucose levels, frequently accompanied by elevated muscle Although the relationship between CHH and haemolymph h t

glucose, have been demonstrated for numerous decapod spe­ glucose concentration has been well documented, the role of y b cies in response to a variety of physiological challenges [Cal­ CHH in blood glucose regulation under physiological condi­

d linecles sapidus (Kleinholz, Havel & Reichart 1950; Santos tions is relatively poorly understood. A diurnal peak in CHH e t

n & Colares 1990), Chasmagnathus granulala (Schmitt & San­ concentration and corresponding elevation of haemolYrnph a r tos 1993), Carcinus maenas, Orcanecles limos us (Santos & glucose levels have been reported in 0. Iimasus (Kallen, g

e Keller 1993a), Gecarcoidea nalalis (Adamczewszka & Mor­ Abrahamse & van Herp 1990), and the time course of these c

n ris 1994) and Cardisoma hirlipes (Adamczewszka & Morris peaks suggests a causal relationship. Cancer pagurus experi­ e c 1996)]. Such hyperglycaemia is a common response to envi­ i ences a peak in haemolyrnph CHH concentration during the l

r ronmental or functional hypoxia, and is thought to be trig­ first 30 min of air exposure which precedes a more slowly e d gered in many cases by the action of crustacean developing hyperglycaemic response (Webster 1996) and n

u hyperglycaem ic hormone (CHH) on various target tissues again the temporal relationship indicates that the hypergly­

y (Figure I). Evidence suggests both monoamine stimulated caemia is CHH dependent. In C. magisler there is an abrupt a

w CHH release leading to hyperglycaemia and also direct increase in perfusion of the anterior aorta at the onset of e t hyperglycaemic effects of5-HT and OA independent ofCHH emersion (Airriess & McMahon 1996) which reflects the a

G elevation (LUschen el al. 1993). increase in haemolymph flow through the same vessel after t e CHH is synthesized within the X-organ of the optic gan­ pericardial infusion of OA (Figure 10; Airriess & McMahon n i glion and transported axonally to the sinus gland, located 1992). Hyperglycaemia also develops throughout a 6 h emer­ b a beneath the ganglionic sheath on the surface of the medulla sion period. Given that subsidiaries of the anterior aorta pro­ S

y terminalis in the base of each eyes talk (Cooke & Sullivan vide the primary haemolymph supply to the sinus glands, it is b 1982). There are no significant extra-eyestalk sources of tempting to suggest that changes in arterial perfusion brought d e c u d o r p e R 98 S. Afr. J. Zool. 1998,33(2)

A 0.30 _ Intact 4 _ Control -" ~ Ablated :: 025 ~ Emerscd 0 S g 0.20

~ "0 1l 0.15 ~ 10.10 "0 ~ 0.05 0 ::r: 0 2 3 4 5 0.00 Sham -7 -, Time (h) ~ B Log [5-HT] .~'" Figure 11 In Gecarcoidea natalis 5-HT increases haemolymph [glu­ e~ 0.5 cose] both in the presence and absence of the eyestalks, suggesting ~ "f that this amine can indirectly affect liberation of intracellular carbo­ '= 0.0 I ..c: hydrate stores, mediated by factors released from the sinus glands "- ~ 0 + 30 60 90 and also has direct effects on glucose mobilisation. 5-HT and saline "0 control solutions were injected into the venous haemocoel at the S Time (s) '" base of one ofthe fourth walking legs; after 30 min a venous haemo­ ..c:'" C lymph sample was obtained and assayed for [glucose]. Eyestalks 1:: were removed from cold-anaethsctised crabs at least 72 h before '"0 4.0 experimental use of ablated animals (Kilham, B.G., Airriess, C.N. & ~ '"0 2.0 I '1: Morris. S. in prep). J!l ..: 0.0 I I I . , !, ", I , , , , , , 1 1 , , '" • that there are monoamine receptors in the crustacean sinus . 0 1 2 3 4 5 )

9 glands that promote CHH release but also receptor popula­

0 + Time (min)

0 tions associated with target tissues containing carbohydrate 2 Figure 10 (A) Haemolymph [glucose] increases over 5 h of experi­ stores which can, when activated, liberate intracellular stores d e t mental emersion in Cancer magister (Airriess 1994). Haemolymph and contribute to changes in circulating glucose levels. It is a

d flow through the anterior aorta increases rapidly during (8) emcrsion logical, therefore, that the interaction between neurohor­ (

1 r and (C) following pericardial infusion of to J.unol.l- octopamine mones and CHH must be important both in determining nor­ e

h (indicated by arrows; after Airriess & McMahon 1992, 1994). The mal tonic levels of blood glucose, and in regulating glycaemia s i l anterior aorta carries the primary supply of haemoiymph to the eye­ in response to the metabolic demands imposed by physiologi­ b

u stalk sinus glands, and thus would preferentially direct monoamines cal challenge. P released from the pericardia! organs to these glands. e Artificial elevation of haemolymph glucose decreases cir­ h t culating levels of CHH but increases in lactate increase y haemolymph CHH concentration (Figure 12; Santos & Keller b about by OA might be part of an integrative response, facili­ d 1993b). CHH-containing neurones in the X-organ of Cancer e CHH

t tating the release of from the sinus glands and (or) its borealis are hyperpolarised by glucose, with a Km of 0.25 n distribution to distal target organs and leading to general a I

r mmol.l- suggesting sensitive negative feedback regulation of

g hyperglycaemia. haemolymph glucose levels (Glowik, Golowasch, Keller & e c There are conflicting reports on the role of monoamines in Marder 1997). Not only do these studies imply that glucose n e regulation of the hyperglycaemic response in crustaceans. For c and lactate independently influence CHH release but also that i l example, recent reviews claim that dopamine acts both to the provision of fuel for routine aerobic metabolism (driven r e reduce blood glucose by inhibiting CHH release (Sarojini et by blood glucose) and for the accelerated glycolysis of anaer­ d n al. 1995) and, conversely, that it promotes hyperglycaemia obiosis (responding to lactate) are under separate but interac­ u

y (LUschen et af. 1993). The ability of monoamine neurohor­ tive control. Extreme hyperglycaemia seen in response to a mones to raise circulating glucose levels in bilaterally eye­ physiological stress may be a passive result of the elevation w e t stalk·ablated decapods also seems controversial, or at least of intracellular glucose levels to maximise the gradient sup­ a species-specific. Recent evidence suggests that 5-HT is capa­ porting glycolysis; however, the resulting hyperglycaemia G t ble of increasing the haemolymnph glucose (Figure II) by should eventually lead to down-regulation of glucose mobili­ e n i mobilising muscle glycogen of G. natalis in the absence of sation, both into the blood and in the cytosol. b a the eyestalk sinus glands. However, the 5-HT induced hyper­ Muscle and mid-gut gland stores of lipid and protein may S

y glycaemia is more pronounced in non-ablated crabs (Kilham, be energetically important during different seasons depending b B.G, Airriess, C.N. & Morris, S. in prep). Thus it seems likely on diet and food availability. Lipids comprise a major portion d e c u d o r p e R S. Afr. J. Zool. 1998,33(2) 99

400 It is well known that changes in temperature are associated A with alterations in heart beat frequency and ventilation rate in 300 crustaceans. Until recently, however, there has been a lack of 200 detailed knowledge of the responses and associated mecha· nisms mediating cardiovascular adjustments to temperature 100 stress. However, in semi-isolated heart experiments the tachycardia associated with increased temperature was small o -t---... ::..a.,..f-!!.::;..::::-...-....,---., in comparison to that in intact animals, while a concurrent o 25 50 75 100 125 150 decrease in stroke volume leads to an overall decline in car­ Injected Glucose (rng·kg·') 2000 diac output (De Wachter & Wilkens 1996). This is in contrast B to the increase in cardiac output observed in intact crabs, 1500 , • often despite a decrease in stroke volume (DeWachter & 1000 McMahon 1996a; DeWachter & Wilkens 1996), and suggests • the involvement of exogenous modulators in the superficially 500 • • simple cardiovascular responses to temperature change in whole animals. Neuroamines, particularly octopamine, have been impli­ o 25 50 75 100, 125 150 cated in the response to acute temperature decrease Injected Lactate (rng'kg' ) 150 (Kuramoto & Tani 1994). Interestingly, increased electrical 120 • c activity in the segmental nerves, leading to neurohormone • • release from the pericardiai organs, was greatest at the onset 90 • •• • of experimental temperature decrease. In a longer duration 60 • protocol no clear cbanges in neurohonnone concentration 30 • were detectable in response to a decreased temperature (DeWachter ef al. 1997). Under hypoxic conditions there O+-=-....,----.--.-~-_,r__, was, however, a significant decrease in OA along with a large o 20 40 60 80 100 120 increase in DA concentration associated with hypothermia, Injected Lactate (rng·kg") indicating that a modulation of the suite of responses to tem­ Figure 12 Data abstracted from Santos & Keller (1993b) implicating perature fluctuation is required to deal with the superimposed

. circulating lactate and glucose as regulators of CHH and thus challenge of environmental hypoxia. As with segmental nerve )

9 haemolymph hyperglycaemia in Carcinus maenas. Glucose and lac­ activity, changes in haemolymph flow through the sternal 0

0 tate were injected into crabs, and [CHH] and [glucose] then deter­ artery are most pronounced at the onset of experimental 2 mined. Panel A demonstrates that [CHH] is elevated in response to changes in temperature (De Wachter & McMahon I 996a), d e t lowered haemolymph glucose; panel B that increasing [L-Iactate] suggesting that sensitive temperature receptors ex ist in the a

d (simulated anaerobiosis) elevates (CHH]; and panel C that increas­ aquatic species studied. In terrestrial crustaceans the effects (

r ing [L-Iactate], most likely via CHH, promotes hyperglycaemia. of temperature changes are more acute, owing to the poor e h thermal capacity of air relative to water. This problem is off­ s i l set somewhat by the normally stenothermal habitats of land

b of the mid·gut gland with the highest values occurring in ter­ u restrial crabs where neutral lipids constitute 60% of the total crabs but may pose an additional burden to amphibious crus­ P

e (Morris, S., Hughes, J. & Thompson, M., in prep.). Lipid taceans already challenged by the switch between ventilatory h t media (e.g. Greenaway, Morris, McMahon, Farrelly & Gal­ mobilisation occurs during moulting and gametogenesis and y

b thus MIH might also have a role in the control of energy lagher 1996; Morris ef al. 1996).

d metabolism (Kummer & Keller 1993). Patterns of lipid and e Overall, cardiovascular responses to changes in T, must t

n protein utilisation are variable but generally carbohydrate is compensate for the associated changes in respiratory (meta­ a r used before either. Land crabs which are on nitrogen-limited bolic) demands if they are to be considered adaptive. Impor­ g

e diets, and therefore can not afford to use protein unless criti­ tantly, direct effects of increased Tb and thus increased c

n cally starved, must accumulate non-protein stores to support metabolism include acidosis (the neutral point of water varies e c migratory activity, If CHH is also involved in the control of i ...j),014 pH units.K·'), facilitating 0, unloading at the tissues, l

r lipid metabolism (Santos, Nery, Keller & Goncalves 1997) changes in protein configuration resulting in decreased Hc·O, e d this implies a further level of integration by the family of affinity (Figure 8) with similar results and reduced solubility n

u sinus gland peptides. of respiratory gases. The latter may decrease 0, capacity of

y the haemolymph but for a given amount of 0, unloaded will a w Temperature and behavioural thermoregulation encourage a higher PO, and facilitate diffusion into the tis­ e t sues. Integration at this level must be achieved through evolu­ a The body temperature of crustaceans (Tb), since they are ecto­ G thermic, is dependent on the ambient temperature (T J. Thus tionary changes accommodating these phenomena rather than t e metabolism and activity tend to be directly affected by through short-term phYSiological compensations, although n i the latter surely occur in response to acute temperature b changes in T" although the effect of temperature is usually of a change.

S different magnitude on various components of metabolism.

y Species in thermally variable habitats must have an integrated Behavioural hypothermia, whereby an animal selects a b

d suite of compensatory responses to temperature fluctuation. lower TO' has the important potential advantage of lowering e c u d o r p e R 100 S. Afr. J. Zool. 1998,33(2)

metabolic demand in poikilotherms. Where 0, supply (above) they remain good candidates not only as messenger/ becomes limiting, moderate hypothermia can be beneficial in transducer molecules but as integrative elements of a com­

(i) reducing 0, demand, (ii) increasing the oxygen affinity of plex behavioural response. Recent findings of O2 and the respiratory pigment, and (iii) avoiding metabolically monoamine sensitive nerve cells in ganglia of crustaceans expensive increases in cardiac and ventilatory activity. (Hempel el al. 1996; Massabuau & Meyrand 1996; Figure 2) The crayfish Carnbarus clearly selects a lower T, under suggest an integrative mechanism requiring some considera­ hypoxic conditions (Dupre & Wood 1988) as does the shore ble further investigation. crab, Carcinus rnaenas (De Wachter el al. 1997). The 0, Despite the deficiencies in the models there are strong threshold for stimulating 'hypoxia induced behavioural hypo­ cases presented suggesting that the balance between 100% thermia' (HIBH) appears to relate to the functioning of the aerobiosis and the initiation of anaerobiosis is a crucial condi­ respiratory pigment. Progressively more extreme hypoxia tion and may provide some signal for HIBH. However, if it (decline of 0, signal) can be considered the proximal cause can be shown that HIBH is initiated before recruitment of and the selection of a lower T, the effect, but the relationship anaerobiosis and/or that amines can elicit HIBH in the

between decreasing blood O2 and the translation into initia­ absence of L-Iactate then a different but more informative tion of hypothermia remains largely obscure, possibly involv­ model will result. ing 0, chemoreceptors (Massabuau & Meyrand 1996) (Figure 2). As the ventilatory medium becomes depleted of Ion regulation and water balance oxygen (mild hypoxia) the arterial oxygen saturation is ini­ There are yet further systems that can be influenced by the tially maintained but further reduction in inspired 0, compro­ suite of effectors discussed above, suggesting that many ele­ mises oxygen delivery. The progressive hypoxia would ments ofneurohaemal integration are yet to be elucidated. For normally elicit increased ventilation and often blood per­ example, neuroendocrine control of osmoregulation and ion fusion to sustain O uptake. Decreasing Tb not only reduces 2 balance has been established in principle for many years (e.g O demand but also increases Hc-0 affinity; preserving Pa02' 2 2 Kamemoto & Ono 1969; Kamemoto 1976; Charmantier, The mechanism translating these circumstances (Le. environ­ Charmantier-Daures & Aiken 1984.; Mantel 1985), and mental hypoxia) into a behavioural response, the search for apparently uses primary messengers similar to those pur­ lower Ta. integrating with ventilatory and cardiovascular ported to be involved in respiratory, cardiovascular and meta­ responses remains unclear but attempts to unravel this mecha­ bolic control. Extracts of the pericardial organs (PO) of nism have begun. marine crabs such as C maenas have marked potentiating Injection of isosmotic Na-Iactate into C. rnaenas apparently effects on ion and osmoregulatory activity (Sommer & Man­ induced behavioural hypothermia (DeWachler el al. 1997);

. teI 1988). DA increases both Na uptake and Na'/K'-ATPase ) however, such L-lactate levels are usually associated with 9 activity in C. rnaenas (Sommer & Mantel 1988, 1991) and 0 pronounced hypoxia and significant acidosis. Lactate is 0 stimulates Na'/K!-ATPase in the supratidal Leplograpsus 2 attractive as an integrative signal since it responds to the O2 variegalus (Figure 13; Morris &: Edwards 1995). In both of d e signal, but the involvement of lactate as a primary signal in t these species cAMP has been implicated as a 2nd messenger a HIBH requires persistent hypoxia, with 0, levels weI! below d transducing the up-regulation of transport within the gil! epi­ ( those stimulating behavioural hypothermia. In addition the r thelial cel!s, and the ATPase activity to increase in response e lactacidosis reduces Hc-O, affinity, opposite to temperature. h to lowered salinity (Sommer & Mantel 1991; Cooper & Mor­ s i l Indeed, this may explain the effect of lactate in Carcinus, the ris 1997) implicating salinity activated 2nd messenger sys­ b Hc of which is lactate sensitive. Introducing neutral lactate u tems. Work on isolated perfused gills using membrane P simulates no physiological condition and large increases in permeable cAMP derivatives has linked increased (cAMP) e h Hc-O, affinity will occur; consequently greatly lowering the t directly to increased Na uptake in Callinecles sapidus (Lohr­

y P,O, required to unload sufficient O2, thereby lowering the 0, mann & Kamemoto 1987) and similarly in Eriocheir sinensis b signal. This is consistent with the equilibrium curve model d (Bianchini & Gilles 1990). Importantly, neuroamines stimu­ e t (above). late not only the Na+/K+ ATPase in Eriocheir sinensis gills but n a If lactate were a signal in HIBH, the re-oxidation of lactate also phosphorylation of membrane proteins, possibly the r g

to pyruvate becomes a limiting process and would be slowed A TPase (Trausch el al. 1989). Thus, it appears that neurohor­ e c by the selection of a lower temperature, thus perpetuating the mones such as DA, and possibly others including peptides, n e 0, debt and the required duration of HIBH. It seems intui­ c bind to receptors on the gil! epithelial cel! surface and, via a i l

tively inappropriate that the product of anaerobiosis should be G-protein linked transduction system, stimulate adenylate r e the signal to initiate HIBH for the purposes of avoiding a sys­ cyclase to elevate intracellular cAMP. A common conse­ d n temic shortfall in 0, (and consequent anaerobiosis); instead, quence of elevated (cAMP) is the activation of protein kine­ u

y the suggestion of Tattersall & Boutilier (1997) that HIBH ses and thereby stimulation of protein phosphorylation, a functions to retard lactic acid release seems more likely. consistent with the suggestions of Trausch el al. (1989). w e t Clearly the nature of the HIBH stimulus, the transduction sys­ While it is possible that a membrane protein adjacent to the a tems, and the ecophysiological benefits of this behaviour ATPase rather than the enzyme itself may be the target of G t remain to be resolved. For example, DeWachter el al. (1997) phosphorylation, the end result is the activation of Na'/K'­ e n ATPase and Na transport. In terrestrial decapods such as i suggest that changes in circulating neuroamine concentra­ Bir­ b gus lalro it appears that DA and cAMP act on the same path­ a tions might be involved but the data remain preliminary. S Since these monoamine hormones influence cardiac and ven­ way to bring about a decrease in both ATPase activity and ion y b

tilatory function in crustaceans under hypoxic conditions transport (Morris, Greenaway & Adamczewska, un pub.). The d e c u d o r p e R S. Afr. J. Zoo!. 1998, 33(2) 101

1.4 • • 1.2 .,~ "; Os= 1.0 Q., • 0.8 ..

fused gills (Pierrot, Eckhardt, Van Herp, Charmantier­ Gecarcinid land crabs and terrestrial anomuran crabs of e h Daures, Charmantier, Trilles & Thuet 1994). More recently, marine ancestry frequently have only freshwater to drink and t

y this stimulatory effect of sinus gland extract has been attrib­ must conserve both body water and minimise salt Joss in the b uted to a peptide factor (Eckhardt, Pierrot, Thuet, Van Herp, urine (Greenaway 1988 for review). To this end these crabs d e t Charmantier-Daures, Trilles & Charmantier 1995). Elevated both drink part of their urine and pass the remainder over n

a Na uptake is an essential part of adaptation to freshwater; and their gills so that required salts can be actively reabsorbed r g in the Australian crayfish Cherax destructor, this eyestalk across the branchial epithelium. Under these circumstances it e c factor appears crucial in the pumping response to lowered seems reasonable that branchial ion pumping must frequently n e water (Na) and the maintenance of haemolymph (Na) (Sithi­ run at near maximal rates but may slow if the animal becomes c i l gomgul, Sithigomgul & Morris, unpub.) salt replete from occasional access to salt water. A combina­ r e Therefore, while there is good evidence that biogenic tion of branchial perfusion studies (Morris, Taylor & Greena­ d n amines may directly influence gill epithelium function via a way 1991 for methods) and determination of gill Na'j u cAMP 2nd messenger system the strong possibility that K'-ATPase in the terrestrial anomuran Birgus latro (Figure y a amines may mediate the release of a peptide that also stimu­ 14; Morris, S., Greenaway, P. & Adamczewska, A.M., in w e

t lates ion transport (see energetics sec!ion) must now be inves­ prep) have revealed the appropriate 'offswitch'. Dopamine a tigated. A more sophisticated and diffuse regulatory system and cAMP (10-' mol.l- I circulating) have marked depressing G

t would be consistent with the observation that some effects effects on branchial ion uptake and the associated ATPase e n can be elicited in intact animals but not isolated tissues (Mor­ activity. i b ris & Edwards 1995). a In terrestrial crabs it would clearly be advantageous to reg­ S When placed in dilute (50%) seawater, the marine crab ulate water turnover independently of salt reclamation Gecar­ y b

Cancer magister experiences an increase in heart beat fre- coidea natalis experiences both wet and dry seasons and thus d e c u d o r p e R 102 S. Afr. J. Zoo I. 1998,33(2)

A model of how all of the various physiological systems must be coordinated and integrated during the migration. Seasonal ,-., 16 changes in this species include important modifications to '..r;; 14 both the hyperglycaemia factor within the eyestalks and tis­ -:0/) E 12 sue sensitivity to this factor (Figure 15). Further levels of p:; 10 sophistication must exist in the integrative mechanisms since these seasonal changes are imposed on die I changes 10 0 8 E numerous aspects of metabolism and behaviour. ::l 6 ~ There is tantilising evidence for ontological changes in

~" 4 sensor, messenger, receptor and transduction mechanisms (e.g. Reiber 1997b; Spicer & Morrin 1996) which surely must ""f-<'" 2 -< occur but extend beyond the scope of the present discussion. 0 A more comprehensive understanding of these systems is a Sham Dopam ine cAMP necessary step in future detailed investigation of changes with B development. It is attractive to hypothesise that variation in the circulat­ ~ 450 ing levels of a suite of neurohormones may act to regulate the ~ 400 function of many systems. Consideration of specific segments -Coo of the physiological literature, in isolation of other aspects of -5 350 crustacean physiology, tends to lead to the development of E 5300 oversimplified models. Such simple models can not persist since they require the same primary messengers, at similar ~«: 250 concentrations, to influence differentially a wide variety of ~ disparate physiological processes. The specificity of neuro­ -;; 200 := hormone effects in crustaceans, and particularly the possibil­ " 150 ity of tissue-level modification of neurohormone activity, is "e! an area requiring immediate and substantial attention. ~ 0 Sham Dopamine Clearly, equipped with a contemporary perspective, the investigation of all the discussed aspects of crustacean physi­ Figure 14 (A) The branchial Na+fKl -ATPase in the terrestrial ology must henceforth be conducted under physiological con­ . ) anomuran Birgus lalro is inhibited by circulating dopamine and 9 ditions. Importantly, new information is beginning to show 0 dbcAMP (10--6 moLl- I) as is the uptake of CI- in experiments in 0 how neurohormonal function may be integrated by and 2

which the branchial chambers were artificially irrigated. (B) Impor­ d e tantly, the injection of dopamine elevates endogenous branchial t 0,8 a [cAMP] by more than two-fold, confirming cAMP levels respond to d ~ _ Dry 5ta50n animal ntract ( extracellular dopamine and are invol ved in the down regulation of r 0.7 ~ Wtf ~ason animal ulne' e ion reclamation in land crabs. '0 h s 5 i 0.6 l b variable water availability. While the availability of drinking .e- u o; 0,5

P ~ water has marked effects on urine clearance rate of red crabs 0 e 7 I h (e.g. Greenaway 1994), S-HT (10- mol.l- circulating) signif­ " t = 0.4 :§ y icantly reduces urine clearance and promotes water retention

b ,c (Morris, S. & Ahem, M.D., in prep.). c. 0.3 d

e E t b n 0 0.2

a Higher level integration

r 5 g Throughout this review we have selected examples to illus­ " 0,1 e "

c =: trate how various components of the physiological responses n

e 0,0

c to behavioural and environmental challenge may be initiated, i l Dry Season Animals Wet Season Animals controlled and integrated. Obviously these separate physio­ r e logical responses must be further integrated and modified Figure 15 The effectiveness of eyestalk extracts in eliciting a hyper­ d n within the whole animal. Furthermore, this integration must glycemia response in Gecarcoidea natalis is dependent on seasonal u

y itself be modulated with respect to fluctuating daily require­ variation in environment. Eyestalk extract (onc eyestalk per crab) a ments, season, reproductive state and developmental stage, was injected into the venous haemocoei of crabs collected during the w e t and all will likely differ between species. Each of these is wet season (February 1997) and dry season (June 1997). After 30 a worthy of review but they can not be considered in detail min haemolymph samples were obtained and assayed for haemo­ G t here. lymph [glucose] (Kilham, B.G., AilTiess, C.N. & MOlTis, S. in prep). e n i For example, the annual migratory behaviour of some crus ­ Wet-season animals are clearly more sensitive to eyestalk factors b

a taceans must produce severe physiological demands and than dry-season animals, whilst the eyestalks of the dry-season ani­ S influence both behaviour and physiology. The Christmas mals have less efficacy in inducing hypergJycaemia in both groups y b

Island red crab breeding migration is an obvious illustrative of crabs. d e c u d o r p e R S. Afr. J. Zool. 1998, 33(2) 103

together with peripheral receptors and the CNS. Thus while, BENSON, lA. 1984. Octopamine alters rhythmic activity in the of necessity, increasing both the species database and the isolated cardiac ganglion of the crab, Portunus sanguinolenlus. available experimental models it is clear that resolution of Neurosci. Let. 44: 59-64. BERLIND, A. 1989. Feedback from motor neurones to pacemaker physiological integration in the Crustacea will require the neurones in lobster cardiac ganglion contributes to regulation of marriage of whole animal biology with cellular and biochem­ burst frequency. J expo BioI. 141: 277-294. ical methodologies. BLANCHINI, A. & GILLES, R. 1990. CycliC AMP as a modulator The examples emphasised in this review are a small subset ofNaCI transport in gills of the euryhaline Chinese crab Eriocheir of the many investigations covering most of the major aspects sinensis. Mar. Bio/. 104: 191-195. of crustacean physiology. However, the literature on these BOURNE, G.B. & MCMAHON, B.R. 1989. Control of cardiac topics is diffuse and fractured, often contradictory and largely output and its distribution in crustacean open circulatory systems. uncollated outside of narrow specific fields of study. The syn­ J. Physiol. 418: 134pp. thesis of existing information with new, and different types, BRIDGES, e.R. & MORRIS, S. 1989. Respiratory pigments: of data on crustacean physiology will improve our apprecia­ interactions between oxygen and carbon dioxide transport. Can. 1. tion of the biology ofthese animals and provide general mod­ Zool 67: 2971-2985. els that will contribute significantly to our understanding of BURGGREN, W.w. & MCMAHON, 1lR. 1983. An analysis of scaphognathite pumping performance in the crayfish Orconec(es animal adaptation to environment. virilis: Compensatory changes to acute and chronic hypoxic exposure. Physiol. Zool. 56: 309-318. References BURNETT, L.E. 1992. Integrated function of the respiratory ADAMCZEWSKA, A.M. & MORRIS, S. 1994. Exercise in the pigment hemocyanin in crabs. Amer. Zool. 32: 438-446. terrestrial Christmas Island red crab Gecarcoidea natalis. II. BURNETT, L.E. & BRIDGES, e.R. 1981. The physiological Energetics of locomotion. 1. expo Bioi. 188: 257-274. properties and function of ventilatory pauses in the crab Cancer ADAMCZEWSKA, A.M. & MORRIS, S. 1996. The respiratory gas pagurus. J Camp. Physio/. B. 145: 81--88. transport, acid-base state, ion and metabolise status of the CHARMANTlER, G., CHARMANTIER-DAURES, M.& AIKEN. Christmas Island Blue Crab, Cardisoma hirlipes (Dana) assessed D.E. 1984. Neuroendocrine control of hydro mineral regulation in in situ with respect to immersion. Physiol. Zool. 69: 67-92. the American lobster, Homarus americanus (H. Milne-Edwards, ADAMCZEWSKA, A.M., VAN AARDT W.J., & MORRIS, S. 1837) (Crustacea, Decapoda). 1. Juveniles. Gen. Comp. 1997. The role of lungs and gills in an African freshwater crab Endocrinol. 54: 8-19. Potamonautes warreni (Caiman), (Decapoda, Potamoidea) in gas CHRISTIE, A.E, SKIEBE, P. & MARDER, E. t995. Matrix of exchange with water, with air and during exercise. J Crust. BioI. neuromodulators in neurosecretory structures of the crab Cancer 17: 596-608. horealis.1. expo Bioi. 198: 2431-2439

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