carapace movements associated with ventilation and irrigation of the branchial chambers in the...

J Comp Physiol B (1992) 162:365 374 Journal of Comparative Systemic, Biochemical,

and Environ- mental Physiology B . . . s ~ . o . .

�9 Springer-Verlag 1992

Carapace movements associated with ventilation and irrigation of the branchial chambers in the semaphore crab, Heloecius cordiformis (Decapoda: Brachyura: Ocypodidae) David P. Maitland*

School of Biological Science, University of New South Wales, P.O. Box 1, Kensington, N.S.W. 2033, Australia

Accepted October 29, 1991

Summary. Carapace movements in crabs are briefly re- viewed. While on land and recirculating branchial water, the Australian semaphore crab Heloecius cordiformis (Decapoda: Ocypodidae), a semi-terrestrial air-breathing mangrove crab, sequentially depresses and elevates its carapace relative to its thorax (0.5-1 mm excursion) in a regular pump-like manner. In quiescent crabs each carapace-pumping cycle lasts about 4 s; carapace depression takes 3 s and elevation 1 s. Carapace movements are brought about by pressures generated within the branchial chambers by the scaphognathites, probably in combination with carapace muscles. Carapace movements are associated with bilaterally synchronised scaphognathite activity. Unilateral scaphognathite activity was not observed. During normal forward recirculation of branchial water the scaphognathites beat at about 1.5 Hz (slow-forward pumping) and the lungs (epibranchial chambers) are not ventilated. In Heloecius, the lungs are not physically separated from the gills below by an anatomical barrier. Lung ventilation is accomplished during the following sequence of events: the carapace is lowered and the scaphognathites pump in a fast-forward mode at about 2.8 Hz. This activity preferentially pumps air out of the lungs and generates suction within the branchial chambers (4-10 cm H20 below ambient) which draws water from external body surfaces into the hypobranchial space below and around the gills. At the end of the carapace's downward travel the scaphognathites switch from fast-forward to fast- reverse beating at about 4 Hz. This pumps air into the lungs and the carapace elevates. As a result, during carapace elevation the water which had previously been drawn into the branchial chambers by fast-forward pumping activity is released and flows out between the legs and into the abdominosternal cavity. When the car-

Abbreviations: FF, FR, SF, SR, fast-forward, fast-reverse, slow- forward, slow-reverse scaphognathite pumping; MEA, Milne Ed- wards aperture

* Present address: Department of Physiology, Medical School, University of the Witwatersrand, Parktown, Johannesburg, South Africa, 2193

apace reaches its original resting or "up" position the scaphognathites switch from fast-reverse to slow- forward beating to re-establish water recirculation through the branchial chambers. This cycle is subsequently repeated. In stationary crabs, there are 2 carapace-pumping cycles per minute, increasing to 14 per minute in active crabs (walking). When water is absent, the lungs are preferentially ventilated by slow-reverse scaphognathite pumping activity. Carapace movements do not occur in the absence of branchial water. Carapace pumping is thought to provide a mechanism which per- mits the scaphognathites to ventilate the lungs in the presence of recirculating branchial water, without this water interfering with lung ventilation or being lost to the environment.

Key words: Carapace movements - Lung ventilation Scaphognathite - Water circulation - Crab, Heloecius

Introduction

Except at each moult, the carapace of most crabs remains relatively immobile. Several species of amphibious land- living grapsids, however, possess a loosely attached, highly manoeuvrable carapace. M/iller (1869) reported that it was possible to see inside the branchial chambers of a small grapsid, Aratus pisonii, as it "lifted" the posterior margin of its carapace away from its body, and observed similar movements in two other grapsids, Sesarma sp. and Cyclograpsus sp. Verwey (1930) reported that regular carapace movements occurred in Sesarma mederi (=S. taeniolata), S. meinerti, S. bataviana, S. nodulifera, Grapsus strigosus and Metopograpsus lati- frons. Macnae (1968) and Alexander and Ewer (1969) observed carapace movements in the grapsids Sesarma meinerti and S. catenata. In addition, Macnae (1968) noted that the carapace of Sesarrna meinerti could be raised and lowered in a lopsided fashion/either the right or left side only, or both together.

366 D.P. Maitland: Carapace movements in Heloecius

Despite the above observations, the function of carapace "lifting" in amphibious land-living crabs has re- mained unclear. Both M/iller (1869) and Verwey (1930) believed it allowed air to enter the gill chambers, while Verwey (1930) also suggested that the aperture thus formed allowed water to return to the branchial chambers posteriorly after flowing over the dorsal carapace [in those crabs that possess such a circulatory route; Alexan- der and Ewer (1969); Felgenhauer and Abele (1983); Santos et al. (1987)]. Verwey (1930), however, was uncer- tain as to whether this later function was simply collat- eral to the apertures ' main function of allowing air into the branchial chambers.

Besides grapsids, few other crab species have been observed to make any significant movements of their carapace outside the moulting process. Passing reference to carapace movements have been made for the following species: the freshwater crab Potamon granulatus, the ocypodids Ilyoplax delsmani and Metaplax elegans (Ver- wey 1930), and the gecarcinid mangrove crab Ucides cordatus (Santos et al. 1985). Outside the Brachyura, non-moult ing carapace movements have been observed in the mud lobster Thalassina anomola (Pearse 1911), the hermit crab Coenobita clypeatus (McMahon and Burg- gren 1979), the robber crab Birgus latro (Harms 1932; Cameron and Mecklenberg 1973) and the marine lobster Homarus americanus (Wilkens and M c M a h o n 1972).

The semaphore crab Heloecius cordiformis (Ocypodi- dae) lives on mangrove mudflats in south-east Australia. Semaphore crabs are similar in appearance to fiddler crabs, and the two are closely related (Tfirkay 1983). Semaphore crabs are active at low tide in air; their branchial chambers are modified for both air breathing and water circulation (Maitland 1990a, b). Water held within the lower regions of the branchial chambers is primarily used for feeding (Mait land 1990a, c). This water is continuously pumped out of the branchial chambers by the scaphognathites over specialised setae-bearing regions of the carapace and back through the branchial chambers over the gills (Maitland 1990b). The upper regions of the branchial chambers are expanded and lined with a vas- cular epithelium to form air-filled "lungs". The lungs, however, are not separated f rom the gills (which lie below) by an anatomical barrier such as is found, for example, in the soldier crab Mictyris longicarpus (Mait- land 1987; Farrelly and Greenaway 1987). Use of the term "lung" to describe the epibranchial chambers of Heloecius seems appropr ia te in view of the crabs ' depen- dence on aerial respiration. Semaphore crabs appear to be obligate air-breathers, extracting up to 80% of their oxygen needs via their lungs (Maitland 1990a). The respiratory behaviour of these crabs while within their burrows at high tide is unknown, al though the closely related ocypodid Uca sp. is known to tolerate considerable periods o f hypoxia within its burrow (Teal and Carey 1967).

While on land and recirculating branchial water, He- loecius performs a regular and elaborate sequence of carapace "pumping" movements . Without carapace movements , semaphore crabs appear unable to ventilate their lungs adequately (Maitland 1992) and, due to the

reduced nature of the gills and poor gill function (Mait- land 1990a), are unable to maintain normal aerobic metabolism (Maitland 1992). Oxygen consumption consequently drops by 38% and whole body lactate rapidly accumulates. In addition, cardiac frequency drops by 32% (Maitland 1992).

In the present paper carapace movements are described in detail, while their functional role in lung ventilation is investigated in the accompanying work (Mait- land 1992).

Materials and methods

Animal collection and maintenance. Male and female semaphore crabs Heloecius cordiformis (males 1.0-7.7 g; females 1.0-4.0 g) were collected from mangrove swamps around the southern end of Botany Bay, Sydney, Australia. Crabs were maintained as described previously (Maitland 1990b).

Experimentalproeedures. All experiments were carried out on unrestrained crabs. All crabs were allowed at least 24 h to recover from electrode implantation, lung cannulation and the attachment of a carapace-movement monitoring device. All crabs (except where stated) had access either to air alone, or to air and a thin layer of seawater (about 3 mm in the base of their holding container) where indicated.

Carapace movements. Carapace depression and elevation (relative to the thorax) was monitored by means of a capacitive position- sensitive device (Sandeman 1968). Larger individuals (~ 4 g) of both sexes were used. Two insulated ledges (L-shaped brass sheet, 0.2 mm thick) were glued using cyanoacrylate cement (Superglue), to the posterior margin of the carapace and the 1st abdominal segment (Fig. 1). The sensors (sheet brass, 6 x 8 • 0.2 mm) were glued to these ledges. A short step-shaped wire arm was soldered to the carapace sensor such that when the wand was attached to the wire arm its tip was positioned mid-way between the two sensor plates (Fig. 1). Although the wand and carapace sensor were fixed relative to each other, the abdominal sensor was free to move relative to the carapace. Thus, as the carapace moved down, the two sensors were brought closer together and a corresponding signal change was recorded. Linearity of this signal change was not tested. Because signal noise and drift were a problem, particularly when crabs were active, these traces were not used to measure carapace movement distance. Output was fed to a Gilson IC-MP amplifier and 5/6H chart recorder.

Carapace

L-shaped ledge

insulation sensor sheet

T

i to Diff. Amp.

to Sig. Gen.

to Diff. Amp.

Abdomen

Fig. 1. Diagram showing the attachment of a capacitive position- sensitive device to the rear of the carapace of Heloecius in order to monitor carapace movements relative to the thorax. The rear of the crab is drawn here in profile, with the legs removed (s). Diff. Amp., differential amplifier; Sig. Gen., signal generator

D.P. Maitland: Carapace movements in Heloecius 367

Left lung pressure (cm H20 )

Carapace movement

towering

Right lung pressure (cm H20 )

Time (s)

~ I -5

- 10 4~

carapace pumping Act ive

F i g . 2. Simultaneous recording of left and right epibranchial chamber (lung lumen) pressures and carapace movement in Heloecius. The crab was initially stationary and then became active (walking) as indicated. The carapace is normally held in an elevated or "up" position and is subsequently lowered about 1 mm against the thorax during each carapace pumping cycle. Branchial water was present

Branchial chamber pressure. Air pressure changes within the epibranchial chambers (lungs) were monitored with Statham P23BB pressure transducers and recorded as described elsewhere (Maitland 1990b).

Seaphognathite andheart activity'. Scaphognathite activity was monitored by measuring impedance changes (Hoggarth and Trueman 1967) between the bared tips of two fine (0.007 in) Teflon-coated silver wires (A-M systems, USA). The bared wire tips were inserted through very small holes which were formed by pricking the cuticle with the tip o fa 21-G needle. Wires were inserted on either side of the scaphognathites. Care was taken to avoid penetrating the ep- idermis prior to the insertion of the wires. The wires were cemented in place with Superglue. BioScience FC-109 Impedance modules were connected to a Gilson 5/6H polygraph chart recorder via BioScience A100 coupler units.

R e s u l t s

While carrying and recirculating branchial water, semaphore crabs depress and elevate their carapace in a regular pump-l ike fashion (Fig. 2). The f requency o f these movements varies with activity, being slowest in stationary crabs and highest in active crabs (Fig. 2). In stationary individuals, carapace movement s occur at the mean rate o f one cycle every 31 .5+5 .29 s ( • n = t 0 different individuals). Carapace movements increased to a mean o f one cycle every 4 . 2 + 0 . 3 6 s ( • n = 10 crabs) dur ing rout ine activity (walking). The fas- test rate observed in voluntar i ly active crabs was 30 c y c l e s - m i n 1. The initial m o v e m e n t made by the carapace f rom its "rest ing" posi t ion is downward . On av- erage, it takes over 3 s for the carapace to lower (3.26_+0.35 s; • n = 10), bu t less than 1 s for it to rise back to its original posi t ion (0 .98• s; • n = 10). This sequential carapace depression and eleva- t ion is here collectively termed the "carapace pump" .

The carapace-pumpin 9 cycle

Dur ing normal forward recirculation o f branchial water while crabs are in air, the scaphognathi tes beat at a mean frequency o f 1.48+__0.11 Hz (+_SEM; n = 2 0 crabs). This SF scaphognathi te beating typically generates a slight negative pressure within the branchial chambers o f between - 0 . 5 and - l can H 2 0 below ambient. The following events, which take place dur ing each ca rapace-pumping cycle, are summarised in Fig. 3.

As the carapace is lowered towards the cepha lo thorax the scaphognathi tes cont inue to p u m p in a forwards direction but at abou t twice the usual " rout ine" SF frequency (2 .82+0.08 Hz ; • n = 2 0 ; Figs. 2, 3). This F F beating pumps air out o f the epibranchial chamber

I s 3 s i I

0 I I

i ,

Lung _ i pressure ~E Hu~'%~" Et ,' (ca

- i P I f

- 6 ', , i i I

, S l o w - f o r w a r d

l Scaphognathite } - - - " - ~ 1 Fast- f o rw a r d activity

] Fast-reverse i l

Carapace , , -0.5 I 1 movement

(mm) 'r i ', i

-1 Fig. 3. Diagram summarising the scaphognathite sequence associated with a typical carapace pumping cycle. The lung pressure cycle shown is the same for both branchial chambers


Left lung pressure (em H20 )

Carapace movement

lowering I

R htun0 I pressure (cm H20)

Time (s) ~ f t f f f f / ~ r f t t f f t f / ~ f f f f f f r f

Fig. 4. Simultaneous recordings of left and right epibranchial chamber (lung lumen) pressures and carapace movements in Heloecius. In this example, insufficient water was present within the branchial chambers for typical recirculation. Full carapace depression and elevation only occurs during periods of bilateral FF scaphognathite activity (solid curved arrows). Where SR scaphognathite activity on one side coincides with FF activity on the other side, carapace depression does not occur (star, middle trace)

("lung") - bubbles appear at the exhalant apertures - and generates large negative pressures within the branchial chambers i.e. between - 4 and - 1 0 cm H20 below ambient (Figs. 2, 3). This suction draws water circulating externally over various body surfaces into the branchial chambers primarily through the MEAs, but water may also enter through gaps formed between the legs and carapace. On entering the branchial chambers the water collects around the gills as described previously (Mait- land 1990b).

From its original resting position the carapace is pulled down a distance of between 0.5 and 1 mm depend- ing on the crab's size. At the bottom of the carapace's range the scaphognathites switch from FF to FR pumping (Figs. 2, 3) and the carapace begins to "lift". Sca- phognathite frequency increases during FR activity to a mean of 3.82 4-0.15 Hz (4- SEM; n = 20) and pumps air into the lungs.

As the branchial chambers re-pressurise and the carapace rises, the water that had previously been drawn into the chambers during the carapace-down phase begins to exit via gaps which form between the legs and carapace. Much of this water subsequently flows out between the legs, where it forms menisci between adja- cent meral segments. Water also falls, under the influence of gravity, down beneath the crab's body where it is caught by the abdomen as it extends slightly away from the sternum (direct observation). This water flows into the abdominosternal cavity (Maitland 1990b).

FR scaphognathite pumping usually stops and switcher back to SF pumping when the carapace reaches its original resting or "up" position (Figs. 2, 3). Frequent- ly, however, reverse pumping continues briefly, creating positive pressures of + 1 to + 6 cm H20 within the lung (Fig. 2). This has the effect of forcing the carapace slightly further up and displacing more water from the branchial chambers.

At the end of the carapace-pumping cycle the scaphognathites switch back to their normal mode of

SF ptunping. Water is subsequently pumped out of the exhalant apertures and is recirculated as a continuous film over branchial and external body parts as described elsewhere (Maitland 1990b). The above sequence of scaphognathite activity and carapace movements is repeated with each carapace-pumping cycle (i.e. with each episode of lung ventilation).

Bilateral scaphognathite activity

When Heloecius carries and recirculates branchial water the scaphognathites are continuously active. Pauses, or apnoeic episodes, are normally rare, although a brief pause of about 1 s was occasionally observed at the end of some carapace pumping cycles. While left and right branchial pressures and overall scaphognathite activities are closely matched, precise bilateral scaphognathite phase coordination was not observed.

Transitional pumping activity

Without branchial water carapace pumping stops altogether and scaphognathite activity is reduced. How- ever, a complex relationship was found to exist between scaphognathite activity and carapace movements when crabs were denied access to an external water source and were placed in a transitional situation where, although some water was present within the branchial chambers, it was insufficient to be recirculated as a continuous film over branchial and external body parts (Figs. 4, 5). In such situations the discontinuous film of water leaving the exhalant apertures was carried along by gas bubbles. The proportion of bubbles progressively increased as branchial water evaporated until water recirculation stopped altogether.

In the example shown in Fig. 4, the left branchial chamber (top trace) is primarily ventilated (with air) by


Left lung pressure (em H20 )

Carapace movement


Time (s)

,, i '

SR

Active

Fig. 5. Simultaneous recordings of left and right lung lumen pressures and carapace movement in Heloecius. As in Fig. 4, although water was present within the branchial chambers it was insufficient to be freely recireulated. Thus, during quiescent periods the lungs are seen to be ventilated by SR scaphognathite beating in the absence of carapace pumping activity, However, during activity the lungs are ventilated by cycles of carapace pumping (see text for further details)

Left lung pressure (cm H20 )

Carapace movement

lowering


Time (s)

" , ' , ' r l t , ' , ' , ' t . ' , ' , 'dr t , ' . ' . ' , ' t , 'd, ' r~r~tr .rrr~.r~rrr t t t rdrr t ,

-5

FF FR

0-

-5

-10

R2 m SF

Fig. 6. Simultaneous recordings of left and right lung lumen pressures and carapace movement in Heloecius. In this example the crab is active and is recirculating branchial water. Here, the left scaphognathite delays in switching to FR scaphognathite pumping (bars, top trace). Instead of switching from FF to FR pumping as occurs during typical carapace pumping cycles, the left scaphognathite switches to SF pumping. As a result, the carapace does not return to its original position (solid curved arrows, middle trace). R1 and R2 indicate the point of onset of FR activity on the right and left, respectively. Note that during periods of SR pumping on the left (SR top trace) carapace movements do not occur (large arrow, middle trace) despite the generation of reduced branchial pressure on the right by forward scaphognathite pumping (star bottom trace)

sequential episodes of SR scaphognathite beating. As air is pumped into the lungs pulse pressures of + 2 cm H 2 0 are produced (SR, top trace). The right branchial chamber (bottom trace), however, is sequentially evacuated and re-pressurised in a manner similar to that found during cycles of conventional carapace pumping. Full carapace depression and elevation only occurs periodi- cally (middle trace), and apparently only when lung evacuation occurs simultaneously in both branchial chambers (solid curved arrows). Thus, whenever right- lung evacuations (bottom trace) coincide with left-lung

pressurisations (top trace), significant carapace movements do not occur (star, Fig. 4).

Figure 5 shows a similar situation (transitional pumping activity) to that described in Fig. 4, but in another individual. When the crab was quiescent, both lungs were ventilated by episodes of bilaterally uncoordinated SR activity (Fig. 5, open arrows, SR). No carapace pumping cycles occurred during this phase. During a period of activity (walking), a series of carapace depression and elevation accompanied by bilateral lung evacuation and pressurisation cycles occurred. Also in this example, as


in Fig. 4, where one lung is evacuated (bottom trace, solid curved arrow) while the other remains pressurised due to SR activity (top trace, solid curved arrow), then full carapace depression does not occur (bar, middle trace).

A further distinct scaphognathite/carapace activity pattern is illustrated in Fig. 6. This trace shows two instances where the left scaphognathite switches to SF pumping instead of to FR pumping at the end of carapace lowering (Fig. 6, bars, SF top trace). As a result, the left lung remains at a reduced pressure for an extended period. During this period of left scaphognathite SF pumping, the right scaphognathite switches from FF to FR pumping as is more typical (Fig. 6, lower trace, straight arrow, R1). The carapace elevates during right FR activity but before reaching its "up" position, it is subsequently lowered as the right scaphognathite begins a further FF /FR cycle (Fig. 6, middle trace, curved solid arrows). This time, however, right FR pumping activity is accompanied by left FR activity and the carapace rises back to its normal "up" position (Fig. 6, top trace, straight arrow, R2).

The delay of one scaphognathite in switching to FR beating following a period of FF beating was never observed to last longer than the period occupied by two complete pumping cycles.

Figure 6 also shows an example where one scaphognathite pumps in reverse (SR, top trace) while the other pumps forward (star, bottom trace). As a result, the carapace remains in its "up" position (large arrow, middle trace).

Discussion

Carapace movements in semiterrestrial and terrestrial crabs have previously been described as carapace "lifting" movements (Mfiller 1869; Verwey 1930; Alexander and Ewer 1968; Little 1983). In Heloecius the carapace is not "lifted" but depressed. In other words, the initial movement the carapace makes is not a lifting movement but a lowering movement (Figs. 2, 3). Under casual observation the carapace of Heloecius only appears to be lifting because the rising phase is three times more rapid than the lowering phase. Thus, while it is easy to see the carapace lifting, it is often difficult to notice the carapace slowly being pulled down.

Mfiller (1869) suggested that carapace movements in Sesarma were brought about by inflation of the pericardial sacs (with haemolymph). In Heloecius, the pericardial sacs were never observed to be involved with the carapace movements described here; a Perspex window implanted within the branchiostegite failed to reveal cycles of pericardial sac inflation and deflation associated with carapace movements. In addition, my own observations of carapace movements in several species of Sesar- ma and Leptograpsus failed to reveal any link between the pericardial sacs and carapace movements. Thus, it seems probable that the pericardial sacs are not involved in the non-moulting carapace movements of Heloecius. They may, however, be involved in producing carapace

movements at ecdysis (Bliss 1963, 1979; Hartnoll 1982, 1988; Cameron 1985).

At this stage it is not clear exactly how carapace movements in Heloeeius are brought about. Several lines of evidence suggest the possible combined involvement of branchial chamber pressure and carapace muscles [e.g. median dorsoventral, attractor epimeralis; Glaessner (1969)] attached between the thoracic skeleton (en- dophragmal skeleton) and the dorsal carapace.

Perhaps the simplest explanation for carapace movement generation would be that the negative pressure generated within the branchial chambers by the scaphognathites sucks the carapace down (as a result of atmo- spheric pressure pushing on the carapace). While this suction may contribute to a lesser or greater extent to carapace movements (e.g. small carapace oscillations in Fig. 4, star, middle trace), these pressures are not ex- clusively responsible for the observed movements for at least three reasons. Firstly, carapace movements can occur in the absence of scaphognathite activity. When startled or during handling, semaphore crabs immediate- ly cease all scaphognathite activity and simultaneously lower their carapace. After a few moments the carapace elevates again in the absence of scaphognathite activity. While this behaviour does not form part of the normal ventilation/irrigation cycle it does reveal the existence of an alternative carapace-movement generating mechanism. Secondly, carapace movements occur when the branchial chambers are vented. With both branchial chambers perforated, water continued to be pumped forward in an unbroken stream at SF beating frequencies below about 1.5 Hz. However, on switching to FF beating (above 1.5 Hz) air was observed to be drawn along with the water stream and forward water flow was dis- rupted. As a result, the period of carapace lowering and FF beating was greatly extended to over 10 s (15.7 4- 6.2 s; Y 4- SD; n = 10). Again, a pressure-indepen- dent system for carapace-movement generation is im- plicated. Thirdly, the net degree of carapace movement does not correlate directly with the simple summation of pressures generated within the branchial chambers, as would be expected if the carapace were simply "sucked" down or "pushed" up by branchial chamber pressures. This discrepancy is clearly shown in Fig. 6. At R1 (lower trace), the right scaphognathite switches to FR pumping (which increases right branchial chamber pressure toward ambient) and the carapace is seen to elevate. At the same time the left scaphognathite remains in an SF pumping mode (top trace, SF) which maintains a suction pressure within the left branchial chamber of about - 5 cm H20, and the carapace stops short of its fully "up" position (Fig. 6, middle trace, curved solid arrow). This situation contrasts with a period where negative pressure in one branchial chamber (bottom trace, star) is paired with a slight positive pressure in the other chamber (top trace, SR) and yet the carapace remains in its fully "up" position and not in a position that would represent a balance of the branchial chamber pressures.

Thus, it seems likely that carapace muscles are indeed involved in the generation of carapace movements. While dissection reveals the presence of appropriately located


muscles attached between the carapace and endophrag- mal skeleton, their description and possible role in carapace-movement generation awaits further study.

Although lowering of the carapace may involve a combination of branchial-chamber suction together with contraction of carapace muscles, elevation of the carapace may be accomplished either actively or passively, or by a combination of the two. Passive elevation might occur if the internal hydrostatic pressure of the body is elevated during carapace depression (i.e. by passive recoil). Preliminary measurements of body hydrostatic pressure in fact revealed a slight pressure reduction during carapace depression. The situation, however, is complicated by the fact that as the carapace is lowered the flexible lateral thoracic body walls which form the medial wall of the branchial chambers protrude further into the lumen of the epibranchial chambers [direct observation through implanted Perspex windows; see also Maitland (1990a)]. In this regard, the negative pressures generated within the branchial chambers could aid (by suction) the distention of the thoracic body walls.

Active carapace elevation could be brought about by contraction of muscles which are attached to the lateral thoracic body wall and carapace (unpublished observations). It is worth noting at this point the unusual mechanism of lung ventilation found in the Australian freshwater land crab Holthuisana transversa, which does not move its carapace but alternately displaces laterally its visceral body mass first into one branchial chamber and then into the other. Retraction of the body mass from one branchial chamber (inspiration) is accompanied by distention of the body mass into the opposite chamber (expiration) (Taylor and Greenaway 1979). The point of interest in relation to Heloecius is that in Holthuisana, the thoracic body wall muscles contract alternately (asym- metrically): first one side, then the other. In Heloecius, if the thoracic body wall muscles are involved in carapace elevation, then both sides probably contract together (symmetrically) in a bilaterally synchronised manner, since unilateral (asymmetrical or lopsided) carapace movements were never observed.

The fiddler crab Uca vocans (Ocypodidae) also makes carapace movements which superficially appear similar to Heloecius (personal observation). Like Heloecius the fiddler crab was also not observed to make lopsided carapace movements (personal observation). This situation contrasts with grapsid crabs, where both symmetri- cal and lopsided carapace movements have been observed; Sesarma sp. (Macnae 1968), Leptograpsus varie- gatus, Sesarrna erythrodactyla, Grapsus grapsus and Australoplax tridentata (personal observations). Thus, as a preliminary observation at least, it appears that while grapsids (e.g. Sesarma, Leptograpsus, Grapsus) can exec- ute lopsided carapace movements, ocypodids (e.g. Her loecius, Uca) do not.

The results presented in this paper demonstrate a complex relationship between carapace movements and scaphognathite activity. To date, several coordinated scaphognathite/"system" activity patterns have been documented [e.g. tachycardia with reversed scaphognathite pumping; brief "cardiac arrest" with apnoea

(Wilkens 1981 ; McMahon and Wilkens 1983; Burggren et al. 1985; McMahon and Burnett 1990)]. Also, Wilkens (1981) reports coordination between the scaphognathites and the 3rd maxillipeds in intact crabs. Details of how scaphognathite activity is coordinated with heart and maxilliped activity can be found in the cited work. How- ever, how scaphognathite activity may be coordinated with carapace movements in Heloecius awaits further study.

Branchial water

Semaphore crabs normally carry and recirculate significant quantities of water within their branchial chambers (Maitland 1990b). Branchial water, however, is not es- sential for oxygen uptake, since oxygen is primarily taken up via lungs formed from the vascularised lining of the branchial chambers. For this reason, oxygen uptake remains unaffected by a lack of branchial water, but is seriously reduced in crabs with occluded lungs (Maitland 1990a).

While the gills and branchial water play a minor role in oxygen uptake, the gills may still be important for water and ion regulation and acid-base balance (Mantel and Farmer 1983 ; Burnett 1988). These functions would be facilitated by a constant recirculation of water through the branchial chambers. In other air breathing crabs, the gills remain the dominant site for CO2 excretion while in more terrestrial species significant CO2 excretion may also occur across the lungs (Morris and Greenaway 1990).

The importance of water in the lives of semaphore crabs is reflected, not only by the fact that these crabs are rarely seen without recirculating branchial water, but also by the extensive range of morphological and behav- ioural adaptations which are directed toward ensuring its constant circulation and supply (Maitland 1990b).

Bilateral/unilateral scaphoonathite pumpin 9

An unusual characteristic of scaphognathite activity in Heloecius is that unilateral beating was never observed in individuals with branchial water. The scaphognathites were always bilaterally active. In other land crabs which do not recirculate branchial water while on land, frequent scaphognathite pauses and unilateral beating are a common feature of branchial irrigation and ventilation, particularly in inactive crabs (McDonald et al. 1977; Wood and Randall 1981; Taylor and Davies 1982; McMahon and Wilkens 1983; Cumberlidge 1986; McMahon and Burggren 1988).

Scaphognathite activity patterns in the land crab Car~ disoma guanhumi are apparently different from other land crabs (Burggren et al. 1985) and have certain fea- tures in common with Heloecius. Like Heloecius, Car~ disoma usually carries water within its branchial chambers and crabs often spend long periods partially submerged in water, either in their burrows or elsewhere (Burggren et al. 1985). In Cardisoma, scaphognathite


pauses are generally infrequent and of brief duration. Unilateral scaphognathite beating was rarely seen (Burggren et al. 1985). Burggren et al. (1985) rule out the possibility that the constant, bilateral irrigation observed in Cardisoma was caused by experimental disturbances as suggested by other workers (e.g. McDonald et al. 1977; McMahon and Wilkens 1983). Similarly, in He~ loecius this possibility can be ruled out since crabs were allowed at least 24 h to recover from experimental mani- pulation. In addition, unlike the experiments reported by Burggren et al. (1985), in which crabs were restrained during recording periods, the recordings presented here were obtained from unrestrained crabs. Continuous bilateral scaphognathite beating can therefore be regarded as being the normal preferred mode of irrigation in He~ loecius and perhaps also in other crabs that routinely recirculate branchial water while in air. In Heloecius, in view of the symmetry of carapace-pumping activity, together with the importance of continued water circulation for feeding (Maitland 1990c), it is perhaps a functional requirement that the scaphognathites are bilaterally active.

Reversed pumping and lung ventilation in Heloecius

Since semaphore crabs do not appear to utilise, to any great extent, circulating branchial water for oxygen ex- traction while in air (Maitland 1990a), they must in- troduce air into their lungs (epibranchial regions). This is accomplished by episodes of FR scaphognathite pumping.

Crabs like Heloecius (e.g. Sesarma spp.) possess morphological specialisations to carry and recirculate water through their branchial chambers while on land (Mait- land 1990b). In such crabs, as the scaphognathites pump water forwards out of the branchial chambers, an equiv- alent and compensatory volume of water is automatically drawn back into the branchial chambers through the MEAs (as a result of the cohesive properties of water). In this manner, an unbroken stream of water is continuously circulated over external body surfaces and back through the branchial chambers (Maitland 1990b). Under such circumstances, reversals in scaphognathite beat automatically break the circulation of water, simply because gravity pulls the water away from the entrance to the exhalant apertures which occupy an elevated loca- tion in relation to the MEAs. This water falls and collects around the MEAs and abdominosternal cavity. Similar- ly, normal SF scaphognathite pumping fails to break the water flow because of the design characteristics described above. However, above a certain frequency (about 1.5 Hz), forward scaphognathite beating (e.g. FF) tends to draw air bubbles with the stream of water.

In Heloecius, scaphognathite reversals are not only specifically coordinated to coincide with the elevatory phase of each carapace pumping cycle, but perhaps more importantly, they are normally preceded by a precise period of FF beating (during which time the carapace lowers and air is pumped out of the lung (Figs. 2, 3). FF beating serves to pump air out of the lung and to draw

in water from outside the branchial chambers. It might be reasoned that if FF scaphognathite pumping moves air out of the branchial chambers and that this air is replaced by water, then there should not be a drop in branchial chamber pressure. There is, however, a drop in pressure during FF pumping, perhaps because the total branchial chamber air volume is greater than the volume of water carried by the crab. For example, the total branchial chamber volume in a 5-g crab is 0.548 ml (Maitland 1990a) while the maximum volume of water that can be carried is only 0.407 ml. In fact, less water is routinely recirculated (0.298 ml) (Maitland 1990b).

During FF scaphognathite beating, the carapace is simultaneously lowered and the visceral thoracic body walls protrude further into the branchial chambers. These actions reduce the air volume of the lung. Subse- quently, scaphognathite reversals pump air back into the lung, the carapace rises, water begins to flow out of the branchial chambers, and the visceral thoracic body walls are drawn in. Lung volume therefore increases back to its original extent. Perhaps carapace lowering and visceral protrusion allow a greater proportional volume of air to be exchanged than would be possible without such movements. At the end of this sequence, normal SF water circulation takes place, during which time oxygen can presumably be taken up from the fresh store of air trapped within the lungs. This proposed air-breathing function of carapace movements is reflected in active crabs by a corresponding increase in carapace-pumping frequency, presumably to accommodate an increased oxygen demand (Figs. 2, 5). This function is further investigated in the accompanying paper (Maitland 1992).

Reversed scaphognathite beating in other crabs

While episodes of reversed scaphognathite beating are rarely seen in land crabs breathing air in the absence of branchial water, e.g. Gecareinus lateralis (Taylor and Davies 1981), Cardisoma guanhumi (Burggren et al. 1985), Sudanonautes (Cumberlidge 1986), it is a common pumping mode in partially submerged crabs while breathing air, e.g. Cardisoma (Burggren et al. 1985), Scylla (Davenport and Wong 1987), and/or when crabs have recently emerged from water onto land (i.e. their branchial chambers retain some water), e.g. Sudano- nautes (Cumberlidge 1986).

In Cardisoma guanhumi reversals occur when the exhalant apertures are placed above water and serve to ventilate the lungs. The introduction of air into the branchial chambers first forces water and then air out via the MEAs (Burggren et al. 1985). Periods of forward pumping (between reversals) serve to pump air out of the lung and draw water through the MEAs. In this way, reversals enable lung ventilation between periods of branchial chamber irrigation. A similar pattern of dual branchial chamber ventilation and irrigation has been observed in Sudanonautes (Cumberlidge 1986) and Scylla (Daven- port and Wong 1987) when partially submerged in water. Similarly, the pictures published by Taylor and Innes (1988) showing Cardisoma carnifex and Ueides cordatus


sitting in shallow water and bubbling air through their branchial chambers suggest that these crabs also ventilate and irrigate their branchial chambers in a manner similar to that found in Cardisorna guanhumi.

In Heloecius, scaphognathite reversals function to ventilate the lungs and in the presence of branchial water are almost always associated with carapace movements. Although there is very little information regarding carapace movements in other land crabs where carapace movements have been observed, most authors have com- mented on the fact that carapace movements do not occur if water is absent from the branchial chambers (M/iller 1869; Verwey 1930; Macnae 1968; Alexander and Ewer 1969). Similarly in Heloecius, carapace movements do not usually occur if branchial water is absent. The significance of this curious feature of carapace movements is discussed in the accompanying paper (Maitland 1992).

Acknowledgements. I thank Professor David C. Sandeman for sup- port during my tenure as a Dean's Postgraduate Scholar at the University of New South Wales. D.C. Sandeman was supported by grants from the A.R.G.S. I thank Ross Foertmeyer for translating Verwey. This paper, and its author, have greatly benefited from the input of an anonymous referee.

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