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THE FUNCTIONAL ANATOMY OF THE DIGESTIVE TRACT OF ASHRIMP METAPENAEUS BENNETTAE RACEK & DALL*(CRUSTACEA: DECAPODA : PENAEIDAE)

[Manuscript received October 17, 19661Summary

The anatomy of the proventriculus, digestive gland, midgut and its diverticula,and the rectum is described. In structure and function the proventriculus is similar tothat of anumber of other Decapoda. Two distinct cell types occur in the digestive gland,a secretory type, and a mucopolysaccharide-containing type, whose function is notclear. The digestive gland has no intrinsic muscles, and depends on extrinsic muscles,and possibly ingested water, for filling and emptying. The midgut extends to thesixth abdominal somite and faecal material is contained in a peritrophic membrane.Evidence for secretory functions of the midgut and anterior and posterior diverticulais discussed. The rectal lining is formed into six longitudinal pads which are used toexpel long sections of peritrophic membrane containing faeces.

Methods of feeding are described. Permeability of the anterior proventriculusto 22Na and [14C]glucose was measured; 22Na approached equilibrium in.6-7 hr,but [14C]glucose passed through at about one-seventh this rate, indicating that directglucose uptake from the proventriculus would be negligible. Food, labelled withparticulate llOAg,was found to begin leaving the proventriculus almost as soon as itwas filled, but complete emptying took 6-12 hr. Defecation was at a peak 5-8 hrafter food ingestion, but continued up to 20 hr. The rectum appears to have theadditional function of pumping water into the gut via the anus.

While detailed studies of the functional anatomy of the digestive tract of a numberof Decapoda Reptantia have been carried out, e.g. Astacus (Huxley 1884; Balss 1927),Cancer (Pearson 1908), Nephrops norvegicus (Yonge 1924), Galathea (Pike 1947),knowledge of Natantia is meagre. Patwardan (1 9 3 5 ~ ~935b) described the structureand mechanism of the gastric mills of various shrimp, and Pillai (1960) studiedthe whole digestive system of Caridina laevis. Although there have been somephysiological investigations of Penaeidae (MacFarland and Lee 1963; Dall 1964,1965a-1965d), none has dealt specifically with the digestive tract. Dall(1965c) treatedsome aspects of carbohydrate content of the digestive gland and also (1965d) presentedevidence for excretion of calcium via the anus. Other studies have been confined topurely morphological features. Kubo (1949) and Dall (1957) used the "stomodoealapparatus" for taxonomic features, and although Young (1959) published a mono-graph on the morphology of Penaeus setiferus, most of it concerns musculature andthe section on the gut is brief.

* Formerly M. mastersii (Haswell) (see Racek and Dall 1965).t Department of Zoology, University of Queensland, Brisbane; present address: Universityof Guelph, Ontario, Canada.

Aust. J . Zool., 1967, 15, 699-714

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In the present investigation attention has been confined to morphology and his-tology of the gut, an d the m anne r in which the food is treated by the respective regions.No study of digestion and absorption, apart from proventriculus permeability, hasbeen made. Nevertheless, from th e diverse nature of food eaten, it would seem that,as in Nephrops, a full complement of the usual enzymes is probably present (Yonge1924). The musculature a nd a rm atu re of the proventriculus in Penaeidae have beendescribed in detail by Kubo (1949) and Young (1959), and only the histology andoverall functions are dealt with here. The mo uthpar ts of Metapenaeus are similar tothose of most other genera within the family, and are not described here (see Kubo1949 (various genera); Yo ung 1959 (Penaeus setiferus)).

Animals were collected by trawling in Moreto n Bay, Queensland. All wereadults of 14-20-mm carapa ce length (D all 1958), and only actively feeding intermoultshr imp were used. Holding tan ks were main tained at 20-25OC, with salinity 35%,.Food was normally given two or three times per week, but no food was given for2-4 days prior to experimen ts. All experiments were carried ou t at 20C, with watersalinity 35%,, unless otherwise stated.

Tissues were always fixed directly fro m living animals. Ge neral fixatives usedwere formol-saline, Heidenhain's Susa, Zenker (P antin 1946). F or cytological detailof digestive gland, midgut and its diverticula, an iso-osmotic, osmium tetroxide,buffered fixative was used consisting of 5 ml barb ital buffe r; 16 ml filtered sea waterof salinity 35%,; 5 ml 0 . IN HC l; and 0.2 g 0 s 0 4 ; final pH of solution 7 .4 ; fixationtemperature 4 C (modified from Pease 1960). Tissues were fixed for 20-30 min.Formol-saline at 5OC gave best results for the digestive gland, which is notoriouslydifficult to fix before autolysis begins, which may cause artifacts giving the appearanceof sloughed-off cells. G oo d fixation was obtained with the osm ium tetroxide fixativeonly with pieces of tissue less th an 1 mm thick. All tissues were embedded in paraffinand cut at 7-10 ,u. Stains employed were Mayer's haemalum, Mallory's (Pantin1946); histochemical methods used were Feulgen reaction for DNA, periodic acid-Schiff (P.A.S.), an d toluidine blue for polysaccharides (Pearse 1961).

The Radiochemical Centre, A mersham, supplied Z2NaCl an d [W ]g lu co se asstock items, and llOAg was obtaine d from the Au stralian Atom ic Energy Com mission.Specific activity of the latter w as ab out 1 mc per 400 mg A gN 03 . Finely dividedsilver was produced by reducing a dilute solution with hydroquinone and thoroughlywashing the precipitate. Particle size ranged up to 10 p, but most particles were1-5 p. Counting was carried out with an EKCO 645A ratemeter with scintillationhead, o r with an E KC O 664A scintillation counter and N530F autoscaler.

(a ) Anatomy of the Digestive TractFigure 1 shows the general organization of the gut. A short oesophagus opensvertically into a large anterior chamber, followed by a smaller posterior chamber

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DIGESTIVE TRACT OF METAPENAEUS BENNETTAE 701

partly su rround ed by the digestive gland. The cuticular lining of the foregut ends atthe junction of the posterior chamber an d midgut. The tubular m idgut extends fromthe thorax to the anterior region of the sixth abdom inal somite, and like the anteriorand posterior diverticula, is lined by columnar epithelium. Proctodoea l cuticlelines the rectum up to its junction with the midgut an d posterior diverticulum.

Fig. 1.-Lateral dissection of the complete digestive tract. AC, Anterior chamber of proventriculus;AD, anterior diverticula; pco,opening of posterior chamber of proventriculus into digestive gland;MG, idgut; PD, osterior diverticulum; R, ectum; A, anus; T, telson; MO, outh; o, oesophagus;a-a, 6-b, c-c, d-d, e-e, represent the planes of the transverse sections shown in Figures 2, 4, 5,8, and 7, respectively.(i) Proventriculus (Figs. 2-5)

The terminology of this structure is in an unsatisfactory state. AlthoughPearson (1908) objected to the use of "cardiac" an d "pyloric" for anterior andposterior chambers respectively, this misleading nom enclatu re has persisted. Theuse of the term "stomach" for the anterior cham ber is also to be condemn ed; thestomach functions more as a crop. K ub o (1949) referred to the complete foregutstructure as the "stomodoea l apparatus", bu t the less clumsy "proventriculus" hasbeen mo re generally accepted. As indicated in Figure 1, the chamber into which theoesophagus opens, an d which has a function analogous to the cro p of many insects,is referred to here as the "anterior chamber" (Fig. 2). The posterior opening of thischamber is closed by the complex armature of the gastric mill (Kubo 1949; Dall1957). Triturated fo od passes into the dorsal compartment of the posterior chamber(Fig. 4). Only the finest particles ar e able to pass via the complex setose "presses"of the ventral com par tmen t to the openings of the digestive gland (Fig. 5). Largerparticles which are excluded are apparently free to pass directly from the dorsalcompartment to the midgut.

The lumen of the oesophagus is occluded by an anterior and two lateral foldswhich run fo r the grea ter part of its length. The oesophagus is constricted by con-traction of a band of circular muscles round the oesophagus pressing the folds

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702 W. DALLtogether. Since the folds are filled with loose connective tissue their arrangemen tpermits maxim al distension of the oesophagus during food ingestion. Such a narrangement is necessary since the oesophagus is lined by relatively inelastic cuticle.The cuticle (Fig. 3) is about 10p thick and the underlying epidermis consists ofdensely staining columnar cells.

Fig. 2.-Transverse section of the anterior chamber of the proventriculus through theoesophagus (Fig. 1, section a-a). M,Muscles; CM,ircular muscle layer; AC, nteriorchamber; OES, lumen of oesophagus; CON,circumoesophageal connectives; MD ,mandible; EP, epistome, containing glands.Longitudinal folds also run along the sides of the anterior chamber of theproventriculus permitting expansion of the chamber if it is filled with food. Tw opairs of longitudinal ridges in the floor of the chamber form channels which leadback to the digestive gland openings in the posterior chamber. The m ost median pairof ridges form a single small median channel in the a nterior pa rt of the chamber, b ut

posteriorly these ridges becom e confluent and the channel is obliterated. The lateralridges adjacent to the median ridges form open channels anteriorly, but projectinwards posteriorly so as to enclose the median ridges, and become continuous withthe ridges dividing the posterior chamber into dorsal and ventral compartments.

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DIGESTIVE TRACT OF METAPENAEUS BENNETTAE 703These longitudinal ventral channels running fo rward fr om t he digestive gland probablycarry enzymes to th e food in the anterior chamber (Yonge 1924; Pike 1947).(4 (b)

Fig. 3.-(a) Lining of oesophagus. ( b ) Lining of anterior chamber of proventriculus.E, Epicuticle; P, procuticle; ED, epidermis; c, connective tissue; M, muscle.

The cuticle of the anterior chamber (Fig. 3) is about 5 p, the epicuticle being1-2 p thick. As in the oesophagus, the epidermis is a layer of densely staining columnarcells, and co ntrasts with the attenua ted epidermis of the external body cuticle duringthe interm oult period (Dall 19653). This is further discussed in Section III(b) below.

Fig. 4.-Transverse section through the posterior chamber of theproventriculus (Fig. 1, section b-b). DC, Dorsal compartment;c, connective tissue; M, muscle; vc, ventral compartment; LG,

longitudinal groove between rows of setae.In the posterior chamber the lateral ridges with their dense setae permit onlythe finest particles to pass into the ventral com partment. The large ventral median

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ridge of the latter bears longitudinal rows of dense setae with grooves between themwhere the fine food particles collect, and are then passed backwards to the openingsof the digestive gland (Fig. 5). Normally the dorsal com partment is more or lessBled with food particles of various sizes, but in the ventral compartment food isrestricted to the longitudinal grooves.

Fig. 5.-Transverse section through the openings of the digestive gland into theposterior chamber of the proventriculus (Fig. 1, section c-c). LM , Lappets whichextend backwards into the midgut; DC,dorsal compartment; vc, ventral compartment;OD, opening into digestive gland; s, secondary channel into which digestive gland

tubules open; TO, tubule opening adjacent to proventriculus openings.(ii) Digestive Gland (Figs. 1 an d 6)

The general structure of this organ agrees with the descriptions of Yonge(1924), van Wee1 (1955), an d Pillai (1960). The bulk of the tissue comprises simpletubules whose walls consist of a single layer of secretory epithelium. Only a fewscattered cells an d small blood vessels occur between individual tubules. Som e of thetubules open directly into the region adjacent to the openings of the proventriculus,but others are grouped round secondary channels leading from this region (Fig. 5).The distal ends of the more dorsal tubules meet above the posterior proventriculus,

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DIGESTIVE TRACT OF METAPENAEUS BENNETTAE 705while the mo re ventral tubules meet below it. The tubules are connected by sparseconnective tissue, and the whole organ is invested in a yellow-brown membranewith guanine-like deposits scattered over its surface. Th us the digestive gland com -pletely su rround s the posterior proventriculus.

The apex of each tubule consists of a cuboidal epithelium of closely packedcells which stain intensely a nd which exhibit metachromasy with P.A.S. an d toluidineblue. Immediately below this area is a zone of transitional cells with similar stainingcharacteristics, but which are columnar. The remainder of the tubule consists ofcolu mn ar cells with extensive cytoplasm . Th e upper p art of this region is show n inFigure 6. Two majo r cell types appear to be present. Th e most abun dan t formvacuoles (Fig. 6, vc) which become progressively larger, and ultimately fill and dis-tend the cell. Detached cells were no t observed in properly fixed tissues, an d secretiontherefore appears to be merocrine. Th e other cell type (Fig. 6, MC) has a densecytoplasm and large nucleus, and exhibits metachromasy with P.A.S. and toluidineblue. These cells apparen tly contain a large amou nt of mucopolysaccharide (Dall1 9 6 5 ~ ) .No cells were observed showing graded intensities of metachromasy, nor wasthere any other evidence to support van Weel's (1955) and Pillai's (1960) conceptth at these are merely a stage in a secretory cycle. Miyawake, M atsuzaki, an d Sasaki(1961) report mucopolysaccharide-containing cells which also contain calcium, theam ou nt of the latter fluctuating with the mou lt cycle. Th us there app ears evidencefo r two distinct cell categories, a secretory and a "storage" type, as described byearlier au thor s (see Vo nk 1960). Dav is and B urnett (1964) present evidence that inthe crayfish all tubule cells arise from the embryonic cells of the apex and go throughabsorptive, then secretory and fibrillar stages, and finally atrophy. Th e apical regionof the tubule is adjacent to the haemocoel, and absorption from this region seemslikely. However, holocrine secretion has been described in crayfish (Hirsch andJacobs 1929, 1930), and atrophy of cells may not be a general feature of Decapoda.N o such cells could be distinguished in Metapenaeus. In addition , the digestive glandis generally believed t o play an im po rtan t role in storage in preparation for m oulting(Drach 1939; Rena ud 1949). Ap art fro m a few scattered interstitial cells, tubulecells comprise almost all of the digestive gland, an d any such storage function s mustreside in these cells. However, Dall (1 9 6 5 ~ ) as shown tha t the "storage" cells areabundant immediately after moulting and suggested that they may secrete mucinsinvolved in digestion. Henc e the role of particul ar cells in storage of substance sutilized f or m oulting is no t clear.(iii) Midgut (Figs. 7 and 8)

Tho ugh morphologically par t of th e midgut, th e digestive gland is functionallyclosely associated with the proventriculus a nd has therefore been considered separately.In crayfish and some other Decapoda the proctodoeal cuticle extends almost to theopenings of the digestive gland and the digestive gland is virtually the only portionof the digestive tract obviously derived fro m t he embryonic midgut (Balss 1927). Thelatter author remarks that the midgut varies considerably in length throughout theM alacostraca. Yonge (1924) foun d that the midgut of Nephvops extended for thegreater part of the length of the abdomen, and in Metapenaeus the midgut reachesto the sixth abdom inal somite.

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Fig. 6.-Transverse section of a digestive gland tubule, below thetransitio nal region (see text). vs, Secretory cells form ing vacuoles ofdigestive enyzmes (these vacuoles ultimately coalesce an d distend thecell); MC , cells containing muco polysaccharide; BB , "brush-border";AT, adjacent tubules separated only by a thin layer of connectivetissue.

Fig. 7.-Transverse section thr ou gh the ant erio r midgut (Fig. 1,section e-e). PM , Peritrophic membrane containing faeces; CE,columnar epithelium; LML, longitudinal muscle layer; a circularmuscle layer lies imm ediately inside this; a thin connective tissuecovers the o uter m uscle layer.

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DIGESTIVE TRACT OF METAPENAEUS BENNETTAE 707The midgut is lined throughout its length by dense columnar epithelium whichis surrounded by muscular and connective tissue (Fig. 7). No "vermiform bodies",described as occurring in the posterior midgut of Caridina (Pillai 1960), could befound. A peritrophic membrane is secreted by the anterior midgut. The epithelium

extends into paired anterior diverticula (Fig. 8) and a single posterior diverticulum(Fig. 9). These diverticula open at the terminations of the stomodoeal and of theproctodoeal cuticle, respectively, and appear to be simple extensions of the midgut.

Fig. 8.-Transverse section through the openings of the anterior diverticulaof the midgut (Fig. 1,sectiond-d). AL, Lumen of a diverticulum (the two luminafuse above and below the gut); CUT, cuticle which lines the canal; CAN, canalleading from the foregut (G) to the lumen of the diverticulum; CE , columnarepithelium; LD, lappet which occludes the opening to the diverticulum. (Thecuticular lining of the gut stops just behind the openings to the diverticula.)

The openings of the anterior diverticula are covered by a pair of lappets extendingbackwards from the proventriculus. Food particles were never found in the diverti-cula in sections from many animals, although food was always present in the midgut,and the lappets with their fringing setae therefore appear to function as valves.Particulate matter was also invariably absent from the posterior diverticulum, but thisis accounted for by the presence of the peritrophic membrane in this region.Epithelial cells of the diverticula are taller and more closely packed, and stain

more intensely than those of the midgut, but otherwise the epithelia are similar.There is every appearance that the epithelium of the diverticula is very active, and itis unlikely that the structures are vestigial. It is possible that the diverticula have a

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708 W. DALLsecretory function, and may play a part in excretion of calcium and other salts viathe anu s (Dall 1965d, an d unpublished data). However, the midgut lining also hasth e appearance of a secretory epithelium. In both diverticula an d midg ut, vesiclesform at the bases of the epithelial cells, and seem to be extruded into the lumen.Th e vesicles con tain refractile, non-b irefringent, gran ular , acidophilic material, whichdoes no t stain metachromatically with P.A.S. or with toluidine blue; these structuresapp ear to be similar t o Pillai's (1960) "cytoplasmic bodies". N o definite function asyet can be assigned to these vesicles, but evidence is growing to support the long-established view that the midgut has an excretory function (see Parry 1960).

Fig. 9.-Lateral dissection of the sixth abdominal somite, showing posterior midgut (MP)pos-terior diverticulum (D) rectum (R), and anus (A). T, Telson; RP, one of the six longitudinal

rectal pads (four are shown); NC, nerve cord; u, uropod.(iv) Rectum (Fig. 9)

A t the junction of the midgut an d rectum the epithelium of the form er endsabru ptly , and the six large pad-like rectal ridges begin. These ridges a re filled with aspongy reticular tissue which did no t take up any of the stains used. Posteriorly theridges taper dow n to longitudinal muscle bands. Circular muscles surround therectum, an d their con traction presses the pads together a nd so may close the rectum.The role of the pads and their longitudinal muscles is discussed below.

(b) Functions of the Digestive Tract in Feeding(i) Food Ingestion

The animal normally appears to browse selectively on surface particles oforganic detritus. Th e three pairs of chelate appendages bear tufts of setae whichapparen tly have both taste and tactile functions. F o r example, when the animalencounters a larger piece of food, the chelae rapidly explore the surface before thefoo d mass is seized. Du ring browsing, th e chelae appea r t o search systematicallyover the surface of the substratum, and presumably gather clusters of micro-organ-

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D I G E S T I V E TRACT OF METAPENAEUS BENNETTAE 709isms and other edible matter, which are then conveyed to the mouthp arts. T ha t thisfeeding is selective is indicated by the very small quan tity of inorg anic particles i n thegu t. Larger food m asses are eaten while being held between the external maxillipeds.If the food is tough (e.g. muscular tissue) the maxillipeds assist in detaching piecesby pushing the food mass away while a portion is grasped by the mandibles. Feedingceases when the anterior chamber of the proventriculus is filled, althou gh large foodpieces may be held by the maxillipeds until feeding is resumed. A starved anim al isable to fill the anterio r proven triculus with soft food (e.g. cooke d liver-cereal homo -genate) in less than a minute.(ii) Perm eability of the Anterior Proventriculus

Yonge (1936) found that the proventriculus of Nephrops was permeable to glu-cose. Dall (1 96 5~ ) bserved that [14C]glucose introduced into the an terior proventri-culus was metabolized very rapidly. Th e thin y ti c le of this structure with its apparentlyactive epithelium, noted above, raises the question whether there may be significantabsorption through the proventricular wall.

Proventriculi were dissected out of freshly killed animals, large muscles wereremoved, and the organ was flushed out with iso-osmotic sea water containing 22Naor [14C]glucose. A ligature was then tied just behind the gastric mill, the anteriorcham ber filled to capacity with labelled water, and the oesophagus ligatured. Theprepara tion was washed for 5 min in three changes of iso-osmotic unlabelled seawater, and then suspended by a thread in similar water and stirred continuously.F or 22 N a counting the proventriculus was removed, washed once an d counted ina well-type sodium iodide scintillation crystal. 14C was coun ted by transferring analiquot to a planchet, drying and counting with a methacrylate fluor. Results areshown in Figure 10 where mean values of three experiments with each isotope areshown. 22N avaried at 5 hr from 75 to 90 %, while [X!] glucose varied fro m 6 to 12%at 2 hr. Th e latter experiments were no t continued beyond 2 hr to avoid possibleeffects from bacterial decomposition. Perm eability t o sodium is high, bu t, resultsindicate that permeability to glucose is insufficient to permit a significant amountof digested carbohydrate to be absorbed in this way.(iii) Rate of Food-mass Movement

Anim als were fed cooked , hom ogenized liver-cereal in to which finely dividedllOAg particles had been g rou nd , the mixture being rolled into pellets. Sh rim p werewashed after feeding, placed in plastic gauze tubes, and regions of the gut counted bypositioning the anim al over an 8-mm g ap between two 50-mm thick lead bricks, witha scintillation coun ter below the gap . This metho d obviously does n ot perm it discrimi-nation between adjacent regions, but it was found that passage of food throughanterior proventriculus, digestive gland region, anterior and posterior midgut couldbe detected. Also, there is no measure of digestion since only inert particles are beingtraced. In all, three batches of three animals each were me asw ed. In o ne batch theshrimp were placed in the tubes only for counting, whereas in the other two theywere left undisturbed for the du ratio n of the experiment. No appreciable differencescould be detected.

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710 W. DALLFood begins to leave the anterior proventriculus almost as soon as it is flled,by 2-3 hr there is a marked decline, and by 6-12 hr the chamber is usually empty.The digestive gland area reaches a maximum value 0.5-1 h r after feeding and declinesslowly to zero over a 12-20-hr period. In som e cases there was an ab rup t dro p in radio-

activity indicating that there is a mechanism for emptying the blind tubules of thedigestive gland of indigestible particles. In starved animals some defecation mayoccur from 1 h r after feeding, bu t usually reaches a peak a t 5-8 hr. However, the gutis no t completely emptied of llOAg until 12-20 hr a fter feeding. A large par t of diges-tion would therefore appear to be com plete by abo ut 8 hr, but the total process maytake longer. The upper value of 20 hr is probably m aximal and could representonly the final emptying of indigestible particles.

TIME (HR)

Fig. 10.-Diffusion of 22Na (@) and [W ] lucose (+) through theanterior proventriculus, shown as percentage of radio-isotope in

proventriculus at zero time.

(iv) Mechanims of Food-mass MovementMusculature and operation of the proventriculus is described by Young (1959)for Penaeus setiferus, and Metapenaeus bennettae appears to be similar in all essentialfeatures. Filling and em ptying of the digestive gland m ust be achieved by the actionof the proventricular muscles and the muscles surrounding the gland, since it hasvirtually no intrinsic muscle fibres, nor are there any muscle attachments on thesurface. The complex movem ents of the proventriculus may be seen through thedorsal carapace, and the proventriculus is pushed rhythmically into the digestive

gland. Very fine food particles may be observed in the proximal portions of thetubules, and these could be forced in by the ac tion of the "presses" of the posteriorproventriculus.

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DIGESTIVE T R A C T OF META PENAEU S BENETTAE 711

Larger particles excluded from the digestive gland and residue from the latterare guided well back into the peritrophic membrane of the midgut by the backward-projecting lappets of the proventriculus. These form a U-shaped ch annel much as inNephrops (Yonge 1924). Strong peristaltic contrac tions of the isolated mid gut maybe observed in vitro. These contraction s probably assist in moving the peritrop hicmem brane along in vivo. The rectal pads ap pear to play a n essential par t in defecation.During this process, the rectum contracts a number of times in rapid succession, anda length of intact peritrophic membrane containing faeces, approximately the lengthof the midgut, is pushed ou t. The rectal pads apparently serve to g rip the peritrophicmem brane and as the rectum contracts so a section is extruded. Thus the anim alproduces characteristic long faecal pellets.

IV . DISCUSSIONThe proventriculus of Metapenaeus appears to function in essentially the sameway as th at of Nephrops (Yonge 1924), Astacus (Balss 1927), an d GaIathea (Pike 1947).Yonge (1936) found t ha t the proventriculus of N ephrops was fairly permeable to sodiumchloride, bu t that glucose penetrated "extremely slowly". Results with Metapenaeusshow th at sodium equilibrium would be reached in 6-7 hr. Da ll (1965d) found th atabdo min al cuticle was permeable to 45Ca; the high permeability of the proventricularcuticle to 22 N a is therefore to be expected. Glucose appears to diffuse at abou tone-seventh the rate of 22 N a,an d although this is an appreciable rate, glucose absorp-tion is probably a negligible factor in normal abso rption of digested food. Da ll

(19 65 ~) ound that [14C]glucose introduced into the proventriculus was rapidlymetabolized, an d suggested tha t the glucose may have been absorbed directly from theproventriculus. It is more likely tha t th e glucose was passed rapidly to the digestivegland an d absorbed there, since, in the experiments described above, labelled food waswas detected in the digestive gland a few minutes after feeding.As noted above, filling and emptying of the digestive gland must be due to theaction of the proventriculus an d surround ing thoracic muscles. Yonge (1924) des-cribed circular and longitudinal muscle fibres between the digestive gland tubules inNephrops, but Pearson (1908), Pike (1947), and Pillai (1960) indicated that sparseconnective tissue and blood vessels were the only interstitial tissues in the animals

they examined. Sections of Metapenaeus stained with Mallory's stain revealed a fewfibrous strands between the tubules and these gave a typical collagen blue-stainingreaction. Occasional nuclei were scattered along the fibres. Phase-contra st exami-nation did no t reveal muscle fibres. Nephrops appe ars to be unique in th e possessionof intrinsic digestive gland muscle fibres, an d o ther species so far described app ear t oneed some extrinsic mechanism for filling and emptying the gland. Fo x (1952) recordedoral drinking in a number of Decapoda, and a large water intake has been found tooccur in Metapenaeus (Dall, unpublished data). This water, plus mu scular action,could play an important role in filling and emptying the digestive gland.In addition to th e digestive gland, gut diverticula occur in a num ber of Decapoda

(Calman 1908; Pearson 1908; Balss 1927; Young 1959; Pillai l960), bu t so far nodefinite functio n has been revealed. They a re absent in the freshwater Astacus (Balss

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71 2 W. DALL1927), and functions associated with regulation in the marine environment might bepostulated , were it not for the fact that they are absent in Galathea (Pike 1947). Th ediverticula are particularly well developed in Cancer (Pearson 1908), and the presentauthor has found a similar development in several species of Portunidae, Grapsidae,and Ocypodidae, and it is likely that the Brachyura are all similar in this respect.No diverticula could be detected in the brackish-water shrimp Macrobrachiurnequidens (Palaemonidae), but another caridean freshwater shrimp Caridina laevis(Atyidae) has three (Pillai 1960). Yo ung (1959) described midgut diverticula inPenaeu s setiferus, an d the w riter has foun d them in Penaeu s esculentus an d P.plebejusas well as in Metapenaeus bennettae. A num ber of penaeid species are euryhaline(M acF arla nd an d Lee 1963; Dall 1964), and Metapenaeus bennettae extends intoregions where Macrobrachiurn occurs. It does not therefore app ear likely that, inshrimp at least, the midgut diverticula are organs associated with osmotic regulation.Secretion of digestive enzymes is possibly a function, but this would be unlikely inthe B rachyura, for in these the gut is lined with chitin alm ost from an us to digestiveglan d openings. A possible role in salt excretion has been me ntioned abov e and willbe the subject of a future paper.

Th e midgu t appea rs to be similar to tha t of the Norw ay lobster, Nephrops,(Yon ge 1924), rather than to t ha t of the shr imp Caridina, (Pillai 1960). A peritrophicmem brane has been recorded in various Caridea (F orster 1953), and is probably char-acteristic of those Malac ostraca with a long m idgut, whe re it is a functio nal necessity.Re ctal pa ds ha ve been described in C aridina (Pillai 1960), bu t unlike Metapenaeuswhe re the pads are quite smo oth, spinules are present. Macrobrachium equidens hasrecta l pad s sim ilar to those of Metapenaeus. As well as its role in expelling faeces inthe peritrophic membrane, the rather elaborate rectum also appears to have an im por-ta nt func tion in anal swallowing of water. Fox (1952) described this in a number ofCrustacea, Pillai (1960) made some detailed observations of rectal drinking inCaridina, and D all (1965d) found evidence of uptake of calcium via the an us. Rectal"pum ping" was observed in both Metapenaeus an d Macrobrachiurn when no peri-trophic membrane was being extruded and water intake appeared to be taking place.To what extent this serves to assist in defecation and gut distension as proposed byFo x (1952), or whether it serves some other function, remains to be determined.

Th e author's thanks are due to Miss C. Du nning fo r her assistance in preparingmany of the slides used in this work, which was made possible by a grant from theCommonwealth R esearch Gran ts Committee.

VI. REFERENCESBALSS,H. (1927).-In "Handbuch der Zoologic". (Ed. Dr . Willy Kukenthal.) Vol. 3, Pt. 1.(Walter de Gruyter and Co. : Berlin.)CALMAN, . T. (1909).-In "A Treatise on Zoology". (Ed. Sir Ray Lankester.) Pt. 7, Appendi-culata; Fascicle 3, Crustacea. (Black: London.)

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15/16

DIGESTIVE TRACT O F METAPENAEUS BENNETTAE 713DALL, W. (1957).-A revision of the Australian species of Penaeinae (Crustacea: Decapoda:Penaeidae). Aust. J . mar. Freshwat. Res. 8, 136-230.DALL,W. (1958).-Observations on the biology of the greentail prawn, Metapenaeus mastersii(Haswell) (Crustacea: Decapoda: Penaeidae). Aust. J. mar. Freshwat. Res. 9, 111-34.DALL, W. (1964).-Studies on the physiology of a shrimp, Metapenaeus mastersii (Haswell)

(Crustacea: Decapoda: Penaeidae). I. Blood constituents. Aust. J. mar. Freshwat. Res.15, 145-61.DALL,W. (1965a).-Studies on the physiology of a shrimp, Metapenaeus sp. (Crustacea: Decapoda:Penaeidae). 11. Endocrines and control of moulting. Aust. J. may. Fveshwat. Res. 16, 1-12.DALL,W. (1965b).-Studies on the physiology of a shrimp, Metapenaeussp. (Crustacea: Decapoda:Penaeidae). 111. Composition and structure of the integument. Aust. J. mar. Freshwat. Res.16, 13-23.DALL,W. (1965c).-Studies on the physiology of a shrimp, Metapenaeus sp. (Crustacea: Decapoda:Penaeidae). IV. Carbohydrate metabolism. Aust. J. mar. Freshwat. Res. 16, 163-80.DALL,W. (1965d).-Studies on the physiology of a shrimp, Metapenaeus sp. (Crustacea: Decapoda:Penaeidae). V. Calcium metabolism. Aust. J . mar. Fveshwat. Res. 16, 181-203.DAVIS,E., and BURNETT, . L. (1964).-A study of growth and cell differentiation in the hepa-topancreas of the crayfish. Devl. Biol. 10, 122-53.DRACH, . (1939).-Mue et cycle d'intermue chez les Crustaces Decapodes. Annls Inst, oceanogr.,Monaco (N.S.) 19, 103-391.FORSTER,. R. (1953).-Peritrophic membranes in the Caridea (Crustacea: Decapoda). J. mar.biol. Ass. U.K. 32, 315-8.Fox, B. M. (1952).-Anal and oral intake of water by Crustacea. J. exp. Biol. 29, 583-99.HIRSCH,G. C., and JACOBS,W. (1929).-Der Arbeitsrhythmus der Mitteldarmdriise von Astacusleptodactylus I. 2. vergl. Physiol. 8, 102-44.HIRSCH, . C., and JACOBS,W. (1930).-Der Arbeitsrhythmus der Mitteldarmdriise von Astacusleptodactylus. Z. vergl. Physiol. 12, 524-58.HUXLEY,. H. (1884).-"The Crayfish." (Kegan, Paul & Trench: London.)KUBO, . (1949).-Studies on the penaeids of Japanese and its adjacent waters. J . Tokyo Coll.Fish, 36, 1-467.MACFARLAND,. N., and LEE,B. D. (1963).-Osmotic and ionic concentrations of penaeideanshrimps of the Texas coast. Bull. mar. Sci. Gulf Caribb. 13, 391-417.MIYAWAKE,., MATSUZAKI,., and SASAKI,N. (1961).-Histochemical studies on the hepato-pancreas of the crayfish, Pvocambavus clarkii. Kumamoto J . Sci. B 5, 161-9.PANTIN,C. F. A. (1946).-"Notes on Microscopical Technique for Zoologists." (CambridgeUniversity Press.)

PARRY, . (1960).-Excretion. In "The Physiology of Crustacea". Vol. 1. (Ed. T. Waterman.)(Academic Press, Inc. : New York.)PATWARDHAN,. S. (1935a).-On the structure and mechanism of the gastric mill in Decapoda.V. The structure of the gastric mill in natantous Macrura-Caridea. Pvoc. Indian Acad.

Sci. (B) 1, 693-704.PATWARDHAN,. S. (1935b).-On the structure and mechanism of the gastric mill in Decapoda.VI. The structure of the gastric mill in natantous Macrura-Penaeidea and Stenopidea:Conclusion. Proc. Indian Acad. Sci. 2, 155-74.PEARSE, . G. E. (1961).-"Histochemistry." (J. & A. Churchill: London.)PEARSON,. (1908).-"Cancer (The Edible Crab)." L.M.B.C. Mem. XVI. (Liverpool UniversityPress.)PEASE,D. D. (1960).-"Hi~tological Techniques for Electron Microscopy." (Academic PressInc.: New York.)PIKE,R. B. (1947).-"Galathea," L.M.B.C. Mem. XXXIV. (Liverpool University Press.)PILLAI,R. S. (1960).-Studies on the shrimp Caridina laevis (Heller). 1. The digestive system.

J , mar. biol. Ass. India 2, 57-74.RACEK, . A., and DALL,W. (1965).-Littoral Penaeidae (Crustacea Decapoda) from NorthernAustralia, New Guinea and adjacent waters. Vevh. K. ned. Akad. Wet. (b) 56, 1-119.

8/3/2019 paid paper

16/16

714 W. DALLRENAUD, . (1949).-Le cycle reserves organiques chez les CrustacCs DecapodCs. Ann. Znst.ockanogr., Monaco (N.S.) 24, 259-357.VAN WEEL,P. B. (1955).-Processes of secretion, restitution and resorption in gland of mid-gut(glandula media intestini) of Atya spinipes Newport. Physiol. 2001. 28, 40-54.VONK,H. J. (1960).-Digestion and Metabolism. In "The Physiology of Crustacea". Vol. 1.

(Ed. T. Waterman.) (Academic Press, Inc.: New York.)YONGE, . M. (1924).-Studies on the comparative physiology of digestion. 11. The mechanismof feeding, digestion, and assimilation in Nephrops norvegicus. Br. J , exp. Biol. 1, 343-89.YONGE,C. M. (1936).-On the nature and permeability of chitin. 11. The permeability of theuncalcified chitin lining the foregut of Homarus. Proc. R. Soc. B 120, 15-41.YOUNG, . H. (1959).-Morphology of the white shrimp, Penaeus setiferus (Linnaeus, 1758).Bull. U.S. Bur. Fish. 59 (145), 1-168.