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VIMS Articles Virginia Institute of Marine Science

1973

Digestive-System And Feeding Habits Of Cunner, Tautogolabrus-Digestive-System And Feeding Habits Of Cunner, Tautogolabrus-

Adsprus - Stomachless Fish Adsprus - Stomachless Fish

Labbish N. Chao

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Recommended Citation Recommended Citation Chao, Labbish N., Digestive-System And Feeding Habits Of Cunner, Tautogolabrus-Adsprus - Stomachless Fish (1973). Fishery Bulletin, 71(2), 565-586. https://scholarworks.wm.edu/vimsarticles/648

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DIGESTIVE SYSTEM AND FEEDING HABITS OF THE CUNNER,TAVTOGOLABRVS ADSPERSVS, A STOMACHLESS FISH I,:!

LABBISH NING CHA03

ABSTRACT

The cunner, TIIII(ogo/lIbrus IIdSperSIlS, completely lacks a morphologically or physiologicallydistinct stomach. The alimentary tract consists of the pharynx followed by a shortesophagus with an esophageal-intestinal valve at the junction of esophagus and intestine.The intestine has three limbs and an S-loop. The intestinal bulb where the bile duct entersis present at the anterior end of the first limb. The border between the posterior end ofS-Ioop and the rectum is marked by the intestinal-rectal valve. Histological and histo­chemical observations indicate that the rodlet cells, wandering cells, longitudinal musclelayers, and the rectal valve differ in minor ways from those of other stomachless fishes.Different forms of rodlet cells are found in the bile duct. An alkaline condition (pHvalues between 7.0 and 8.5) prevails throughout the alimentary tract. Alkaline phosphatasereaction was demonstrated only when food was present in the gut. Cunner are carnivorous,and the feeding habits change with growth. Juveniles feed mainly on planktonic crustaceaand adults on sessile animals (mussels and barnacles). The time between ingestion anddefecation of mussels (Mytilidae) by cunner is 10 to 14 hr. Intact mussels can pass throughthe alimentary tract of the fish undamaged and alive.

The most abundant labrid of the New Englandregion, the cunner, Ta utogolabl'ul; adl;pel'l;u.~

(Walbaum), lacks a stomach. The absence of astomach is here defined as the lack of an expan­sion of the alimentary tract between the endof the esophagus and the entrance of the bileduct into the intestine (Figure 1). The mucosaof this region lacks gastric epithelium and gas­tric glands. The alimentary tract is alkalineand lacks peptic digestion. Lack of a stomachappears to be a phylogenetic characteristic ofthe family rather than an adaptive one associ­ated with feeding in this particular species.

The absence of a morphological stomach inteleostean fishes has been recorded in variousspecies of several families, i.e., Atherinidae,Blenniidae, Callionymidae, Cobitidae, Cyprini­dae, Cyprinodontidae, Gobiesocidae, Gobiidae,

I Contribution No. 19, Marine Science Institute, North­eastern University, Nahanl, MA 01908.

"A portion of a thesis submitted to the Departmentof Biology, Northeastern University, Boston, Mass.. inpartial fulfillment of the requirements for the degree ofMaster of Science in Biology, January 1972.

"Virginia Institute of Marine Science, GloucesterPoint, VA 23062. (VIMS Contribution No. 539.)

Manuscript accepted September 1972.FISHERY BULLETIN: VOL. 71. NO.2, 1973.

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FIGURE I.-Lateral view of the alimentary tract of a280-mm SL cunner. E, esophagus; g, gallbladder; I, II,III, sections of intestine; S, S-loop of intestine; L, liver;R, rectum.

Labridae, Mugilidae, Poeciliidae, Scaridae, andSyngnathidae. These families have differentfeeding habits as noted by Ishida (1936),Barrington (1942), Suyehiro (1942), and Al­Hussaini (1947b) and are not closely relatedphylogenetically. Al-Hussaini (1949a) also re­corded different feeding habits among threestomachless species of the family Cyprinidae:Cyprililis carpio, Rutilus rlltillls, and Gobiogobio; they are herbivorous, omnivorous, andcarnivorous, respectively. Physiological lack ofstomach has been noted in various fishes:FllInlulus hete1'oclitus by Babkin and Bowie

565

(1928); Cyprinidae by Szarski (1956); Spher­aides niphables by Ishida (1936); Scaridae andLabridae by Gohar and Latif (1959). Bothmorphological and physiological characters ofthe stomachless fishes appear to be character­istic of the Labridae.

The morpholoy and histology of the entirealimentary tract in the cunner were describedfrom the protrusible lip to the anal papillae.A histochemical study was made on the gut,i.e., the postpharyngeal portion of the alimen­tary tract. Also, feeding habits and habitat,gut contents, and the movement and digestionof food were investigated.

MATERIALS AND METHODS

The fish were collected at East Point, Nahant,Mass., from May to September 1970 and 1971.Larger specimens, over 100 mm SL (standardlength), were taken by hook and line fishingalong the shore, and smaller ones in planktonhauls, by bottom dredging, hand netting, androtenone poisoning in tide pools. Some speci­mens were maintained in constant runningseawater aquaria and fed with mussels (Mytili­dae).

Histological and histochemical studies weremade after starvation (7-10 days) and afterfeeding. Specimens less than 40 mm SL werekilled in 10% Formalin,4 larger ones by severingthe spinal cord and by intracoelomic injectionof Dilantin (sodium diphenylhydantoin, USP)anesthetic (0.1 mll10 g body weight). Tissueswere fixed with absolute acetone, Baker's For­malin, Bouin's (also with seawater), Helly's,Hollande-Bouin's or Zenker's fixatives in orderto demonstrate specific cell types. After fixation,dehydration was done in two ways: the standardmethod of ethyl alcohol or from water toCellosolve (2-ethoxyethanol). Infiltration andembedding were carried out using Steedmanpolyester wax (1960); serial sections were cutat 1 to 8 p. A variety of routine histologicaland histochemical stains were used, includinghematoxylins (Ehrlich's, Galigher's, Heiden­hain's Iron Alum, Groat's) counterstained with

4 Reference to trade names does not imply endorse­ment by the National Marine Fisheries Service, NOAA.

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FISHERY BULLETIN: VOL. 71, NO.2

eosin or fast green, Giemsa (Mallory, 1944, inHumason, 1967), Gomori's trichrome (1950,in Humason 1967), Heidenhain's azan (1938, inHumason, 1967), Masson's trichrome mixture(Gurr, 1956, in Humason, 1967). Histochemicalmethods included: alcian blue (Steedman, 1950;modified by Mowry, 1956, 1963, in Humason,1967), periodic acid Shifrs technique (McMannsand Mowry, 1960, in Humason, 1967), toluidineblue (Lillie, 1929, in Humason, 1967). Acidand alkaline phosphatase tests were done byGomori's modification according to Pearse(1960).

To determine the natural food and feedinghabits, gut contents were examined immediatelyafter capture, or specimens were frozen forsubsequent examination. Also the feeding habi­tat was observed by SCUBA diving. Food move­ment and digestion rates were observed inspecimens from 150 to 200 mm SL whichwere fed whole, small mussels less than 20 mm(shell length), or the visceral mass of largermussels. Cunners were either fed daily or werestarved for 7 days prior to experimentation.Fish were allowed to feed voluntarily on acluster of mussels during the 1/2 - to 1-hr periods.Uneaten mussels and broken shells were re­moved after the feeding period. Carmine,Chinese ink, or ultramarine blue were in­jected into the visceral mass as indicators.Fishes were killed by severing the spinal cordat the base of the skull, at I-hr intervals fromo to 36 hr after feeding. Autopsy was doneimmediately after sacrificing the fish in orderto locate the position of the food. All pH valuesof the gut lumen were determined from narrowrange pH papers.

Ten adults (180-240 mm SL) and 6 juveniles(30-34 mm SL) were used for histological andhistochemical studies, and 68 specimens (30­300 mm SL) for analyses of gut contents.

RESULT

Morphology and Histologyof the Alimentary Tract

As reported by previous authors for otherlabrids (Barrington, 1942; Suyehiro, 1942;Al-Hussaini, 1947b; Gohar and Latif, 1959,

CHAO: DIGESTIVE SYSTEM OF CUNNER

1961), the alimentary tract of the cunner con­sists of neither a morphologically nor a physi­ologically differentiated stomach. The alimen­tary tract can be divided into several regions;the preesophageal cavities, esophagus andesophageal-intestinal valve, intestine, rectalvalve and rectum, and associated organs.

Preesophageal Cavities

This region has three parts: the mouth, buccalcavity, and pharyngeal cavity (Figure 2).

MORPHOLOGY.-Cunners have large ca­ninelike or incisorlike teeth on the premaxillaryand dentary bones. The protrusible premaxillarybears three or four rows of conical teethdirected posteriorly, as are the two or threerows of dentary teeth. The most anterior rowsof both premaxillary and dentary teeth aretwo to four times larger than the other rows.Also, the anterior most teeth are larger thanthe following ones on the same row. Teethfrom 15 specimens (130-230 mm SL) numbered32-66 on the premaxillary and 21-44 on thedentary. The number of teeth increases withthe ~ize of the fish. Developing teeth werefound at the edges of the older teeth on alltooth bearing bones. Longitudinal ridges ofmucous membrane extended from the vomerto the pharynx on the roof of the buccal cavity.

FIGURE 2.-Mouth (M). buccal cavity(B). and pharyngeal cavity (P) of a40-mm SL juvenile cunner (X 40;power of observation). bv, buccalvalve; d, dentary teeth; p, premaxil­lary teel h; T, laSle bud.

The buccal valve is located posterior to thebuccal cavity (Figure 2). There are no teethon the vomer and palatine bones. A large tonguecovers the entire floor of the anterior pharyn­geal cavity and forms a sublingual cavity. Thepharyngeal cavity is bounded laterally by gillarches. A yellowish brown mucous layer, patch­like and thicker than that in the buccal cavity,covers the entire roof and posterior part of thefloor. Strong mucous secreting activities occurin this area. Both the upper and lower pharyn­geal teeth are surrounded paltially by thismucus. The pharyngeal teeth (upper 41-59,lower 28-56) are multitubercular and molari­form. A pair of upper pharyngeal bones attachto the epibranchial bones and a triangularlower pharyngeal plate is attached to the basi­branchial bones.

HISTOLOGY.-The mouth is lined with astratified epithelium of the transitional typewithout a cuticular surface. The mucosa isthrown into ridges which start at the innerside of the protrusible lips (Figure 3) andextend to the esophagus. Taste buds lie on thecrest of the ridge, and basophilic mucoussecreting cells occur at the sides and bases,but the large acidophilic mucous cells presentin the skin are absent here (Figure 3). Poly­hedral cells and low-columnar cells constitutethe rest of the layer. The muco al layer and

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FISHERY B LLETIN: VOL. 71. NO.

FIGURE 3.-Distribution of mucoussecreting cells at sides and base ofthe mucosal ridges of protrusible lipin cunner (X 250, x.s.). a, acido­philic mucous secreting cell; m, baso­philic mucous ecreting cell: mc,mucosal layer: Sm. submucosa.

the ridge are deepest in the region of theteeth where the mucosa may be over 10 cellsthick. Elsewhere, the mucosa is foul' to sixcells thick, except for the sublingual area andthe lateral side of the buccal cavity where athickness of only one or two cells may prevail.The lateral mucosa of the pharyngeal cavity(the internal epithelium of the opercle) is onecell thick and is entirely constructed of mucoussecreting cells attached to the opercle by a thinlayer of connective tissue (Figure 4). The ridgesor mucosal folds are more prominent on themidlines of the roof and floor of the pre-

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pharyngeal regions. There are no ridges on thesurface of the sublingual cavity. The submucosais a layer of fibrous connective tissue underthe mucosa. It is continuous throughout thisregion, and the thickness is closely correlatedwith the depth of the mucosal folds.

Ta te buds occur from the inside of the lipsto the pharyngeal teeth (Figures 3 and 5) andoccasionally are found on the gill arches. Notaste buds were observed on the external sideof lips, anterior sublingual cavity, or the lateralwall of the pharyngeal region. The aggregationof taste buds is closely related to the papi llae

568

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~ .~ J.J- } • ,\, . ,...s:=--:..- ......- ......-=.~ ~ ...... - "';'-'-' -.-..---~ -_.... -

FIGURE 4.-Laleral mucosa or thepharygeal cavity (P) entirely coveredwith mucous secreting cells in cunner(X 250, x.s.). a, acidophilic mucoussecreting cells; c, connective tissue:m, basophilic mucous secreting cell;0, opercJe.

CHAO: DIGESTIVE SYSTEM OF NNER

FIGURE 5.-Taste buds (T) on themucosa of prolrusible lip of cunner(X 400). d. dentary tooth: G, gusta­lOry pore: Sm, submucosa.

folds, i.e., to the middle lines of this regionand to the teeth. The taste bud is an ovoidstructure of epithelial cells (Figure 5). Agustatory pore i' present at the ti p of eachtaste bud. A thickening of the submucosallayer contains the nerve fiber and forms thebase of the taste bud.

Basophilic mucous ecreting cells continuefrom the external lips and appear throughoutthis region. Mucous cells increase in numbersposteriorly. The lateral surface of the pharyn­geal cavity and the ridges among the teethare covered by mucous secreting cells. Beneath

the basal membrane of the mucous layer. thesubmucosa is formed of a thick layer of collagenfiber' toward the posterior part of the pharyn­geal cavity. The areolar connective tissue ofthe tunica propria and submucosa are similarin thi region. Lymphocyte" and granulocytesare apparent in the submucosa of the ridgesamong the pharyngeal teeth. Circular muscleswhich connect to the head bones are externalto the areolar connective tissue.

The epithelium and submucosa of the tongueare similar to that of the pharyngeal cm"ity butare much more compact (Figure G). Posteriorly,

FIGURE 6.-Mucosa (e) and sub­mucosa (Sm) of the tongue of cunnerwith hairlet scnsory organ (X 400).e, cpithelium (mucosa); G, gustatorypore of hairlet sensory organ: m,basophilic mucous secreting cells.

569

the submucosa below the dorsal epithelial layeris thicker than beneath the ventral layer. Af1aplike structure directed posteriorly was ob­served on the ventral side of the tongue. Sen­sory organs, consisting of numerous sensorycells provided with hairletlike processes, occuron the tongue (Figure 6) and open into thepharynx through a gustatory pore.

Esophagus and Esophageal-Intesrinal Valve

Posterior to the pharyngeal teeth, thepharynx constricts markedly to form a short

FISHERY BULLETIN: VOL. 71. NO.2

muscular tube, the esophagus, which opensdirectly into the intestine through a muscularvalve. Distinct longitudinal ridges (Figure 7)continue from the pharynx to the esophageal­intestinal valve and then diverge in the in­testine. There are no transverse connectingcores between the longitudi nal folds. Thesefolds branch shortly anterior to the esophageal­intestinal valve (Figure 8). The mucous cellsin the epithelium disappear in this region(transitional zone). This is more prominent insmall specimens (less than 40 mm SL) thanin larger specimens (200 and 210 mm SL).

FIGURE 7.-Longitudinal ridges of theanterior esophagus of a 40-mm SLjuvenile cunner (X 40, x.s.). ar,areolar connective tissue; cm, circu­lar muscle layer; L, liver; m, mucous;Sk, skeletal l11uscle; sr, serosa; st,st riated muscle.

570

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FIGURE 8.-Transitional zone anterior10 the esophageal-intestinal valve inthe esophagus of a 40-111111 SL cunner(X 40. x.s.). ad, adventitia; CI11,

circular l11uscle layer; g, granulocyte;K, kidney; L, liver; Ill, mucoussecreting cell; Sk, skeletal muscle.

CHAO: DIGESTIVE SYSTEM OF CUNNER

MUCOSA.-The epithelium of the anterioresophagus is a modified transitional type (Fig­ure 9) with large mucous cells extending tovarious depths from the surface. While theesophagus proceeds posteriorly, the stratifiedepithelium gradually becomes simple columnarin the transitional zone between the esophagusand intestine. The flattened nucleus of eachmucous cell is pressed against the base by thelarge vacuole. The mucous secreting cells donot narrow appreciably where they open intothe lumen. They can occupy nearly the entiresurface and thickness of the epithelium, andthey decrease in numbers from anterior toposterior. Also, smaller mucous cells with largevacuoles filled with mucous were found amongthe basal cells in the anterior half of theesophagus (Figure 9). The columnar epitheliumappears gradually while the mucous cells de­crease toward the transitional zone. The largeoval nuclei of columnar cells are located atthe basal level under the level of the mucouscells in the transitional zone. The basal celllayer appears to maintain a uniform thicknesthroughout the esophagus. These cells are smallwith relatively large nuclei. Occasionally, tastebud like structures were found at the tip ofmajor folds in the most anterior part of theesophagus. No cilia are present on the epi­thelium of the esophagus. The mucosal layer

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FIGURE 9.-Mucosa and submucosaof the anterior esophagus of a 200-mmSL cunner (X 400, x.s.). m, mucoussecreting cell; sc, stratum compactul11;st, striated muscle.

of the esophageal-intestinal valve is similar tothat of the transitional zone. except for anincreased number of mucous secreting cells,especially, in the distal portion of the valve(Figure 10).

SUBMUCOSA.-The submucosal layer is anareolar connective tissue between the epitheliumand the muscularis. The stratum compactum(Figure 9) is a layer of compacted fibrousconnective tissue attached to the basal mem­brane of the epithelium. The rest of the areolarconnective tissue i highly vascularized. Longi­tudinal bundles of striated muscles extend fromthe pharynx to the base of the esophageal­intestinal valve in the connective tissue. Also,ill the anterior half of the esophagus, theselongitudinal muscles are dispersed irregularlyup to half of the depth of the folds in the sub­mucosa (Figures 7, 9). Collagen fibers constitutethe framework of the submucosal layer. Thevascular system is scattered in this framework,and leuc cytes, lymphocytes, fibrocytes, andgranular cell are present. The granulocytesfirst appear in the posterior half of the esopha­gus (Figure 8). The submucosa becomes muchthicker on both sides of the esophageal-i ntestinalvalve. Increa ing numbers of granulocytesappear in the submucosa of the intesti nal sideof the valve.

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FISHERY BULLETI : VOL. 71. NO. ~

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FIGURE 10.-The esophageal-intestinalvalve of a 240-mm SL cunner (X 40).E. esophagus: 1. intestine: mf. mucosalfold: sm. smooth muscle: Sm, sub­mucosa.

MUSCULARIS AND SEROSA.-A verythick circular layer of striated muscles con­tinues from the pharynx forming the externalmuscular layer of the esophagus (Figures 7, 8).It is invaded by elements of the vascular systemaccompanied by connective tissue; thus it is aloose rather than a compact layer. This mus­cu lari s appears to decrease in thickness pos­teriorly toward the esophageal-intestinal valve,where it forms a triangular, sphincterlike struc­ture along the base of the valve fold. The basalmuscularis of the valve is formed of smoothand striated muscles and retains significantconnective tissue components. Leucocytes, fibro­blasts, and a few granular cells also occur inthis connective tissue. The distal portion of thevalve contains a single undivided smooth musclelayer (Figure 10). This ring is continuous withthe circular muscle layer of intestine.

The anterior e ophagus is attached to theassociated skeletal muscles by a layer of ad­ventitious tissue. After passing through thetransverse septum, the esophagus separatesfrom the visceral wall ventrally. The dorsalwall of the midesophagus is attached to thekidney and skeletal muscles by a thin layerof adventitia (Figures 7, 8). The ventral side iscovered by the peritoneal lining (serosa) andis separated from the circular mu cularis by avarying thickness of areolar connective tissue(Figure 7). Posteriorly, the serosa increases in

thickness in the vicinity of the esophageal­intestinal valve.

Intestine

The intestine starts posterior to the esopha­geal-intestinal valve and extends to the rectalvalve. The intestine can be divided into' foursections (Figure 1). The fi rst section (1) begi nsdorsally and proceeds posteriorly and slightlyto the left. It turns ventrally and extendsanteriorly to the right as section II. The secondloop curves abruptly posterior at about thelevel of the intestinal bulb. The third section(III) proceeds posteroventrally to an S-shapedloop which is connected by a ShOlt, straightportion of the intestine to the rectum. Intestinalveins from sections I, II, III, and the S-loopare associated with the anterior mesentericvein and the posterior mesenteric vein fromthe rectum (Figure 1). The intestine has aconsistent histological organization throughoutits length with mi nor cytological variations.The mucosa i' more complex in the intestinethan in the esophagus and has zigzag folds aswell as secondary and tertiary folds. The in­testinal bulb is a di lation of the anterior por­tion of the intestine where the latter joins theesophagus. The mucosal fold of the intestinalbulb are deeper than in other portions of theinte tine. There are foul' distinguishable layers

572

CHAO: DIGESTIVE SYSTEM OF C NNER

in the intestinal wall: mucosa, submucosa,muscularis, and serosa (Figure 11).

MUCOSA.-The epithelium of the mucosaconsists mainly of columnar absOl-ptive cellsand goblet cells. The colu mnar absorpti \"e cellsof the cunner are similar to those of thestomach less cyprinids described by AI-Hus­saini (1949a). The epithelium can be dividedinto the same foul' regions: the free border, thesubborder, the supranuclear, and the infra­nuclear zones (Figures 12, 13, 14). The free

FIGURE I I.-Mucosal folds of theposterior section I of the intestineof a 240-mm SL cunner (X 100,x.s.). cm, circular muscle layer; 1m,longitudinal muscle layer; mc, mu­cosa; illS. muscularis; Sm. submucosa;sr I serosa.

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border of the mucosa is sharply definedthroughout the intestine. The striated border(01' subborder) in the active digestive epithelium(Figure 14) is slightly thicker than in theinactive (Figure 13) epithelium. It stains in­tensively with pel'iodic acid-Schiff (PAS) (Figure15) and shows very prominent digestive effectsin the active epithelium (Figure 14). In theresting cell of starved fish, the cytoplasm canbe divided into a subcuticular zone and a layerof fine granules (Figures 12, 13). The sub­cuticular zone in starved fish is a compara-

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FIGURE 12.-Free border (I) of thecolumnar epithelium of the intestine(I) of cunner (X 1,000). gl, granularlayer; go, goblet cell; r. rodlet cell;sb. subborder; sc. subcuticular zone;sp, supranuclear zone.

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FtSHERY BULLETIN: VOL. 71. NO .

FIGURE 13.-The mucosal epitheliumof lhe intestine (II) of cunner (X1,000). am, ameobocyte; g, granu­locyte; gl, granular layer; in, infra­nuclear zone; nz, nuclear zone; p,polymorpho-Ieucocyte; pr, parasite;sb, subborder; sc, subcuticular zone;sp, supranuclear zone.

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SC~Sp

_nz

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prI,

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tively clear region and has a higher affinityfor eosin Y than the other regions. Cell mem­branes are indistinguishable or indistinct re­sulting in a homogeneous appearance. Thegranular layer (Figures 12, 13) continues tothe upranuclear zone and is more basophilicthan other parts of the nonnuclear zones. Inwell-fed specimen, the resting cell. have thesame appearance as in the starved ones. Numer­ous unstained vacuoles are present in the sub­border and the supranuclear zone of the activecells of the absorptive epithelium (Figure 14).In many cases, vacuoles also appeared in the

574

FIGURE 14.-The active absorptionepithelium of the posterior intestine(III) of cunner (X 1,000). bc,basal cells; g, granulocyte; go, goblelcell; in, infranuclear zone; I, Iympho­cytelike cell; sb, striated border (sub­border); sp, supranuclear zone; v,vacuole.

infranuclear zone. The granular cytoplasm ofthe active cells forms a strong basophilic net­work around the vacuoles.

The nuclei of absorptive cells are ellipsoidalwith abundant basophilic granulation and alarge centrally located nucleolus, The nucleiare located at the middle or the basal third ofthe columnar epithelium at the intestinal bulband then gradually move to the upper third ofthe epithelium posteriorly. As a result, thedepth of the supranuclear zone decreases slightlyposteriorly. The nuclei of the developing ab­sorptive cells, th goblet cells, and other non-

CHAO: DIGESTIVE SYSTEM OF CUNNER

FIGURE IS.-PAS demonstration ofgoblet cells (go) in the intestinalepithelium (J I) of cunner (X 1,000).bm, basement membrane; sb, sub­border; sc, stratum compactum.

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Isb

absorptive cells are found always in the infra­nuclear zone. The mucous secreting cells inthe intestine (Figures 12, 14, 15) differ mor­phologically from the mucous cells in the pre­esophagus (Figures 3, 4, 6, 9). They are elon­gate with a thin neck extending to the surfaceand a rod like root extending straight down tothe infranuclear region (Figures 12, 15). Theovoid nucleus of the mucous cell sits at thebottom of this root. Only the mucous secretingcells near the esophageal-intestinal valve ofthe intestinal bulb are the same shape as themucous secreting cells of the esophagus. Mucous

cells also appear to develop in the infranuclearregion and grow or extend gradually to thelumen.

A very distinct type of cell, the rodlet cell,a term introduced by Bullock (1963) for thesecells in salmonids, was also found in the mucosaof the cunner (Figure 12). They are distributedthroughout the intestine but are more abundantin sections II and III. The' are most abundantin the bile duct (Figure 16) and inner epi­thelium of the gallbladder (Figure 17). Theelongate, oval, rodlet cells are usually locatedin the supranuclear region of the mucosa and

FIGURE 16.-The bile duct (bd) ofcunner with abundant rodlet cells(r) (X 400). g, granulocytes; Sm,submucosa.

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FIGURE 17.-Epilhelium in the gall­bladder of cunncr showing rodlelcells (r), vacuoles (v), and digitiformprocesses (d) (X 1,000). n, nuclcusof rodlcl ccll; Sm, submucosa.

FISH ERY BU LLETIN: VOL. 71. NO.2

are in direct contact with the lumen. Thecytoplasm of the rodlet cells (Figure 17) con­sists of many granules with a threadlike struc­ture extending from each granule to the distalend of the cell. These granules are acidophilicand stained deeply with PAS technique. Alarge nucleus is near the base of the cell.Various developmental stages of the rodletcells can be observed in some of the bile ductpreparations.

SUBMUCOSA.-The submucosa, whichfOl'ms the core of the mucosal folds of thp intes­tine, is a single homogeneous layer of fibrousconnective tissue betw en the epithelium and

muscularis (Figure 11). The stratum com­pactum, a thin layer of den e connective tissue,can be identified just beneath the mucosa (Fig­ure 15). The collagenous fibers in the sub­mucosa are more dense at the posterior por­tions of the intestine and rectum. Several celltypes are scattered in the collagenous tissue.The most abundant cells are fibroblast of dif­ferent stages. The young fibroblast has an ovidnucleus and basophilic astral cytoplasm (Figure18). The fibrocytes (mature fibroblasLs) aremost easily seen in the submucosa of the topof the folds. It is very difficu It to see anycytoplasm in these fusiform cells. The nucleiof fibrocyte is elongate or oval in shape with a

576

FIGURE 18.-The submucosa of theintestine of cunner (X 1,000). fb,fibroblasl: fe, fibrocylc: g, granulo­cyle: I, lymphocYlclike ccll; Iy, Iym­phocytc: n. nucleus of granuloeytc.

CHAO: DIGESTIVE SYSTEM OF CUNNER

very dense eccentric nucleolus (Figure 18).Granular wandering cells occur in the mucosa,submucosa, and muscularis (Figures 13, 14,18), and are most abundant in the submuco aat the base of the mucosal folds. In the mucosathey are found in both the supranuclear andinfranuclear zones. These cells are packed withbasophilic granules. The nuclei are alwayspushed to the cell margin by the large granules(Figure 18). Some of the granulocyte presentin the mucosa have very large compact inclu­sion bo lies (Figures 14, 18). The polym rpho­nuclear leucocytes represent one type of wan­dering cell (Figure 13). Its nucleus has two orthree lobes, and there are very fine neutrophilicgranules in the cytoplasm. These leucocyteswere encountered only in the infranuclear zoneand the submucosal layer of the fold. A lympho­cytelike type of cell was encountered also inthe infranuclear zone or the base of the epi­thelium. This type of cell has two nucleoli inthe clublike nucleus and very little cytoplasm(Figures 14, 18). They also were encounteredin the submucosa occasionally. The typicallymphocytes with large nuclei and thin baso­philic cytoplasm were found in the submucosa(Figure 18). At lea t one type of amoebocyte(Figure 13) wa found in the mucosa and sub­mucosa. This type of amoebocyte has a roundnucleu with karyo omes applied to the nuclearmembrane and rays extending from the nu­cleolus which is often eccentric. Numerous

spherical granules and vacuoles occur in thecytoplasm. There are no significant differencesin the distribution or types of wandering cellsin the submucosa throughout the intestine.

Muse LARIS AND SEROSA.-The typi­cal vertebrate muscularis of inner circular andouter longitudinal smooth muscle prevails inthe intestine of the cunner (Figure 11). A verythin layer of smooth, longitudinal muscle fibers(no more than two cells thick) can often beseen inside the circular muscle layer. Thesefibers appear at random in the first three sec­tions of the intestine and become more promi­nent (two to four cell thick) from the S-loopto the rectal valve. A nerve plexus usuallycan be fou nd between the muscle layers. Theserosa is of a more uniform thickness than thatin the esophagus and abuts directly on theextended muscularis.

Reeral Valve and Rectum

A muscular flap valve is present at thejuncture of the intestine and rectum. Therectal valve is formed by a folding of the circularmuscle layer and is not a sphincter valve ofthickened muscularis. The two layers of thefold ar separated by connective tissue (Figure19). Thi' layer of connective tissue containsgranular cells which are more abundant in thesubmucosa of the rectal side of the valve. The

FIGURE 19.-1ntestinal-reclal value ofa 21O-mm SL cunner (X 40, I.s.).cm, circular muscle: I, intestinc; 1m,longiludinal muscle: R. rectum: Sm.submucosa: sr. serosa.

577

nerve plexus, blood vessels, and longitudinalmuscles merge in the connective tissue at thebase of the rectal valve. Some bundles of thecircular layer remain associated with the longi­tudinallayer at the base.

The rectum proceeds posteroventrally to theanus. In the anterior part of the rectum, theabsorptive cells of the mucosa show more vacu­oles in the supranuclear zone in well-fed speci­mens. The submucosal layer has more granu­locytes than the intestine. The vascular systemis also more prominent. The longitudinal musclelayer just inside the circular layer is distinctposterior to the rectal valve. Posteriorly inthe rectum, the number of mucous cells de­creases gradually and then increases aroundthe anus. The epithelium of the rectum con­tinues to the anal papillae (Figure 20). Granu­locytes are the most abundant cell type inboth the internal folds and external papillaeof the anus. The circular muscle layer at theend of the rectum forms a sphincterlike struc­ture. The longitudinal muscles and the nerveplexus radiate into the connective tissue aroundthe anus. The serosa is replaced by an ad­ventitia composed of an extensive developmentof fibrous connective tissue.

Associated Organs

GALLBLADDER-The gallbladder is halfembedded into the liver and opens anteriorly

FIGURE 20.-External surface of theanal papillae of a 210-111111 SL cunner(X 400). a. acidophilic mucoussecreting cell; g, granulocyte; m,basophilic mucous secreting cell; Sm,submucosa.

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FISHERY BULLETIN: VOL. 71. NO.2

into the intestinal bulb via the common bileduct. The bile is usually dark green and haspH values between 7.5 and 8.5. The fullnessof the gallbladder was usually inversely cor­related to the fullness of the intestine. It isa high ly elastic structure which becomes moreelongate when full. The columnar epithelialcells of the mucosa have fingerlike projectionsextending toward the lumen (Figure 17); how­ever, there are no mucosal folds. A smallvacuolelike structure present in each columnarepithelial cell of the gallbladder at the supra­nuclear zone is stained intensively in fastgreen, analine blue, and PAS preparations.Rodlet cells are present and are more con­centrated in the bile duct than in the bladderitself (Figures 16, 17). The submucosa is arather thin layer of very dense collagenoustissue in which a few granulocytes, fibrocytes,lymphocytes, and capillaries are present. Smoothmuscle cells occur beneath the serosa, buttheir arrangement (spiral, random, etc.) couldnot be ascertained. The mucosa and submucosaof the bile duct are similar to those of theintestine; but mucous secreting cells arecompletely absent. The rod let cells in the bileduct increase abruptly in number near itsentrance into the intestine.

P ANCREAS.-The pancreas is diffuse, form­ing small nodules, and consists of numeroussmall lobules scattered with fat and vascular

, .'.1li ...""- t~',- .>d'

CHAO: DIGESTIVE SYSTEM OF CUNNER

tissue in the mesentery (omentum). It is alsodispersed into the liver in the vicinity of thebile duct. Granulocytes are very abundantaround the pancreas and the hepatopancreaticcomplex. The pancreatic duct joins the bileduct neal' the entrance of the latter into theintestine. The mesenteric membranes are moreprominent during late summer when fattytissue accumulates after the active feedingseason.

LIVER.-The liver is divided into threelobes. The central lobe, the largest one, istriangular in shape and the tip continues tothe loop of sections I and II of the intestine(Figure 1). In large specimens this lobe elon­gate posteriorly and covers the spleen ven­trally. Two smaller lobes extend lateral-dorsallyto covel' most parts of the esophagus and theintestine bulb.

Histochemistry

The PAS technique inten ely stains the freeborder and subborder of the intestinal epi­thelium as well as the basal membrane andgoblet cells (Figure 15). The goblet cells andthe granules in the granulocytes and amoebo­cytes give the strongest PAS reaction. Alcianblue and toluidine blue methods stained onlythe mucoid contents of the goblet cells, indi­cating the presence of acid mucopolysaccharide

and mucin. one of the methods showed anysecretory activity by the rodlet cells. Therewere no distinct differences in these reactionsin the different portions of the intestine.

Throughout the alimentary tract the pHvalue ranged between 7.0 and 8.5. Acidic condi­tions were not found in either fed 01' starvedspecimens. Also, acid phosphatase tests werenegative in all cases. Alkaline phosphatasecan be demonstrated at the border of the epi­thelium throughout the gut except anteriorto the esophageal-intestinal valve (Figure 21).No positive reaction for alkaline phosphatasewas found in the epithelium of the gallbladder,bile duct, 01' pancreatic duct. Alkaline phos­phata e activity was intense in the intestinalbulb ami rectal valve, and it was most obviouson the distal surface of the intestinal folds inthe presence of food particles.

Food and Feeding Habits

Cunners at East Point are abundant inshoreduring the summer and may feed intertidallyduring high tide. Cunner were observed swim­ming in the kelp beds and using the kelpsAgc~nult, Ala1'ia, La miI1a1'ia, etc. as shelter.Juveniles (less than 100 mm SL) moved inter­tidally 01' into tide pools where they use brownalgae Ascophylllult and Fucus as shelter. Theintestinal contents of 68 specimens (Table 1)show that the cunner is primarily carnivorous

, . .1.,;)".

v

" (:~\)

," ...

FIGURE 21.-Alkaline phosphatasetest of the esophageal-intestinal valve(V) of a well-fed IBO-mm SL cunner(X 100, 1.5.). E, csophagus; I.intestine.

579

TABLE I.-Gut content of 68 cunners, TIIII {o!<o!lIbrtls

IIdsl'er.\"lIs. from Nahant, Mass.

Standard length (mm) 30-50 100-225 230-300Age group (years old) 0+ -1 + 1 + ·4+ 4 + ·6+5pecimens with food 8 27 10

Occurrences No. % No. % No. 0/0

Mussels (MYlilw, Modioills) 27 100.0 5 50Bivalve larvae 5 18.5Gastropod (Lillori1l0,

Til/as, etc.) 9 33.3 1 10Barnacles (BoI01l1l.\·) 11 40.7 5 50Sea urchin

(Stron!:y/ocentrVlus) 7 25.9 30Crustaceans (amphipod,

3copepod, isopod, etc.) 8 100.0 11.1 1 10Decapod (crabs) 1 3.7 3 30Tunicate (Amarol-lcium) 2 7.4 2 20Polychaete 1 3.7Seaweeds with epiphytic

animals (Bryozoa,9 33.1Hydrozoa, etc.) 12.5 30

Intestinal parasitesAcanthocephala 3 11. 1 3 30Nematode 1 10

during the active feeding season (May to Sep­tember). The foods were mainly mussels My­tilus edulis and Modiolus modiolus, barnacleBalanus balmwides, tunicate Amaroucium sp.,and small specimens of the green sea urchin,Strongylocentrotus drobachiellsis. Entire gutcontents may consist entirely of one speciesmentioned above or, usually, of a mixture ofthese foods. Also some seaweeds, such asChondrus, Laminaria, Polysiphonia, and Por­phyTO, were often associated with the animalfoods. Occasionally, crabs, amphipods, andmicrocrustaceans (copepods, etc.) were found.In juvenile specimens (less than 40 mm SL),amphipods and microcrl1staceans were themain food. The food was well triturated inmost cases although entire mussels (less than20 mm shell length) and, in one specimen, acrab leg longer than the first portion (I) of theintestine (Figure 1) was observed. In aquaria,cunners found their food by sight. They maypick up a whole mussel from the bottom orcatch falling ones as they are introduced intothe tank. Also, they removed small musselsone by one or as batches from clusters. Occa­sionally, the food, as well as mussel shellfragments, was spat out and reswallowed.Feeding activities greatly decreased during thewinter when water temperature in the aquariadropped below 4 °-6 °C. This was especially notice­able in the large individuals caught duringthe previous summer.

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FISHERY BULLETIN: VOL. 71. NO.2

Movement and Digestion of FoodMaterials within the Gut

The gut in unfed cunner had little or nofluid in the lumen. The intestine and rectumwere rather constricted with thick walls. Duringfeeding, small mussels were picked up withthe jaw teeth and triturated by the pharyngealteeth before entering the esophagus. The crushedmussels were pushed back into the eophagusand intestine due to continuous food ingestionduring the feeding period. Feeding continueduntil the food was packed up to the sigmoidloop (Figure 1) and occasionally even to therectal valve or rectum. The intestinal lumendistends and the wall in turn becomes thinnerwhen the gut is full. The shells of one feedingperiod always moved as a unit separate fromthe next feeding period. A period of 10-14 hrwas required for mussel shells from a singlefeeding period (1/2-1 hr) to pass through thealimentary tract. The compact mass of shellsmoving along the intestine sometimes straight­ened the S-loop. Food storage in this stomach­less fish was achieved mainly by the intestineanterior to the S-loop. The loop between sec­tions I and II formed a saclike reservoir(Figure 1). Ingested foods remained in sectionIII longer than in the other loops suggestingthat this section may be responsible for moredigestion and absorption than the other sec­tions. Fluid developed in the lumen duringand for a short while after the presence ofshells. The amount of bile secretion dependedon the quantity of food ingested. The volumescould not be estimated in the present study.In most fish with a full gut which were dis­sected immediately after capture, the gall­bladders were shrunken or contained brownishfluid. The entire range of pH value found in allparts of the gut, both empty and full, was7.0-8.5, thus suggesting alkaline digestion inthe cunner gut.

DISCUSSION

Digestive System

The morphology of the mouth and buccaland pharyngeal cavities of the cunner is similar

CHAO: DIGESTIVE SYSTEM OF CUNNER

to the labrids described by Al-Hussaini (1947b).The buccal valve (Figure 2) is similar to thatof Julis aygula reported by Gohar and Latif(1961), except for the obvious thickening ofthe mucous layer of the anterior surface injuvenile cunners. The rather short relativelength of the gut of the cunner, i.e., the post­pharyngeal portion of the alimentary tract,is about 0.8-1.0 of standard length. The exten­sive vascularization of the serosa and adventitiaof the rectum and the strong alkaline phospha­tase activity of the rectal mucosa indicate thatthis region is very active in absorption and/orsecretion. The S-loop of the intestine may beunique because it was not described for otherlabrids by Suyehiro (1942) and Gohar and Latif(1959, 1961) nor in some other stomachless fishesreported by Babkin and Bowie (1928) andAl-Hussaini (1949a). Bullock (1967) recordeda similar flexure in the posterior portion ofthe intestine of Gambusia affiuis. The S-loopwas somewhat straightened by large amountsof food in the lumen. Alkaline phosphatasetests show weak positive reaction in the S-loop.The significance of the loop may be mechanicalrather than physiological. There are no suc­cessive constrictions of the intestine in cunneras observed by Gohar and Latif (1961) inPseudoscarus harid and credited by thoseauthors to Julis aygula.

Epidermal mucous secreting cells in theepithelium of the alimentary tract of cunnerare mostly concentrated in the postpharyngealcavity and the esophagus and on the analpapillae. These cells have no stalklike elonga­tion at the bottom of the globule nor a narrownecklike structure before the open end (Figures3, 4, 6, 9, 20) as do those of the intestine andrectum (Figures 12, 14, 15). No precise histo­chemical differentiation of these mucous cellswas obtained. These different types of mucouscells have been reported by Al-Hussaini (1947a),Gohar and Latif (1961), Mohsin (1962), Bul­lock (1967), Western (1969), and Bucke (1971)in various fishes. Al-Hussaini (1949b) andBullock (1963), following the terminology ofBaker (1942), described the free border ofthe absorptive columnar cells in the intestineas divided into a superficial layer, a canallayer (or microvilli region), and a granular

layer. These were also distinct in the cunnergut.

The rodlet cells are similar to those dis­cussed by Bullock (1963) in the intestine ofsalmonid fishes and the pear-shaped cell ofAl-Hussaini (1949b) recorded in Gobio gobio.These cells appeared throughout the gut exceptin the anterior intestinal bulb and the posteriorrectum as in Ga mbllsia affiuis (Bullock, 1967).They are also found in the bile duct, gall­bladder, and collecting duct of the kidney ofthe cunner. Bullock (1963) also described theappearance of rodlet cells in the kidney ofCatostomus species. Al-Hussaini (1964) de­scribed the mitosis of the pear-shaped cell inCyprillus carpio. He stated that experimentalevidence indicated the pear-shaped cell mayoriginate from goblet cells in C. carpio andGobio gobio and from wandering blood orconnective tissue cells in Rutilus rutillis. Nocomparable evidence of the division nor originof the rodlet cells was found in this study.Bishop and Odense (1966) proposed that thepear-shaped cell may be a possible enzymesource in the intestine of the cod, Gadus lIIorhua.But the negative phosphatase reactions of therodlet cells in the cunner agree with Bullock's1963 findings for salmonids. Different cyto­logical or developmental stages of rodlet cellswere observed in the mucosa of the bile duct,gallbladder, and intestine. The rodlet cells andtheir empty capsules, which have no distinctnuclei, were partially or entirely free from themucosa of the bile duct. Occasionally, ejectionof granules from the rodlet cells was seen.Rodlet cells have not been described in labridsprior to the present account. The questionremains as to whether they are normal cellsor coccidian parasites (Plehn, 1906).

The submucosal layer of the cunner gutis composed of a rather homogeneous fibrousconnective tis~me. There is neither muscularismucosa nor lamina propria. The stratum com­pactum in various fishes has been discussedby Al-Hussaini (l947a), Burnstock (1959),Gohar and Latif (1961), Mohsin (1962), Bul­lock (1963), and Bucke (1971). In cunner itis a thin layer of regularly arranged fibersimmediately beneath the mucosa. In obliquesections, fibrils can be seen passing from the

581

stratum compactum into the basement mem­brane.

Granulocytes in the submocosa of cunnercan migrate to both the mucosa and the muscu­laris. According to Bolton (1933), basophilicgranule cells occur in vast number in con­nective tissue throughout the gut of salmonidfishes. He suggested that they were histogenouscells developed from mesenchymal cells. AI­Hussaini (1949b) mentioned that two typesof granulocytes also occurred in the intestineof a variety of fishes; some stained blue withGiemsa stain (Tri.r;la hirl/ lido and Sa 111/0 trllfta),and others stained red with Giemsa (Scantssordidus, Rutilus rutilus, Gobio gobio, Athe1'iuaforskali, CyprillUs carpio, Crellilabms melops,and Mulloides aurijlamma). Bullock (1963,1967) stated that the granulocytes had varyingresults in staining reaction according to thedifferent pH value of the stain, which was alsotrue in this study. Large granulocytes, denselypacked with granules which appear purplishwith Giemsa stain, were abundant in the mucosaof cunner (Figure 14); smaller granulocyteswere present which have smaller red staininggranules in Giemsa (Figure 18). In addition,a type of granulocyte was observed in whichthe granules were condensed against thenucleus (Figure 13). Bullock (1963) found cellsintermediate between granulocytes and globuleleucocytes in salmonids but not in Gambusiaaffiuis (Bullock, 1967). This intermediate typecell was found in various levels of the epi­thelium and submucosa of cunner intestine.No precise cytochemical demonstration of thepossible relationships between granulocytes andleucocytes was obtained in this study. Thewandering nature of the granulocytes did notseem to correspond in any way with the foodcontents in the intestine of the cunner. Aggre­gations of granulocytes occurred in the sub­mucosa of the bile duct, rectal valve, and analpapillae of the cunner (Figures 16, 19, 20).Granulocytes similar to those in the intestinewere also very abundant in the pancreas andkidney. The function of granulocytes maydiffer from species to species (AI-Hussaini,1949b). The fine granules of the granulocyteswere stained with PAS in many specimens ofcunner. No evidence that granulocytes help

582

FISHERY BULLETIN: VOL. 71. NO.2

in the absorption and transportation of di­gested foods was found in cunner as reportedfor other teleosts (AI-Hussaini, 1949b; Mohsin,1962). Special aggregations of other types ofwandering cells such as: polymorphonuclearleucocytes, lymphocytes, and amoebocytes werenot found. The presence of amoebocytes (Figure13) with large vacuoles and a large nucleusas observed in this study does not appear tohave been previously recorded.

The muscularis of the esophageal-intestinalvalve (Figure 10) and rectal valve (Figure 19)are formed of circular muscles. Gohar and Latif(1959, 1961) mentioned only one layer ofmuscle fibers in both the esophageal-intestinalvalve and the rectal valve of the labrid Julisaygula. This is true in the esophageal-intestinalvalve of the cunner, but in the rectal valveof the cunner, the circular muscle layer isfolded and the two folds are separated byfibrous connective tissue. AI-Hussaini (1947a,1947b) indicated two separate muscle layersin the i1eo-rectal valve of the stomachlessAtheril/aforskali, and Western (1969) describedthe same arrangement in Cottus gobio. Itwould appear that a more careful analysis ofthe intestinal-rectal (ileo-rectal) valve isrequired.

The differentiation of duodenum and ileumreported to occur in stomach less labrids (Goharand Latif, 1961) was not found in the intestineof the cunner. Histological differentiation ofthe intestine was not mentioned by Curry(1939), AI-Hussaini (1947b), Khanna (1961),nor Bullock (1967) in other stomach less fishes.Thickening of the circular muscle layer at theanterior end of the rectum in cunner was similarto that in other species of stomachless fishes(Dawes, 1929; AI-Hussaini, 1947a, 1947b;Khanna, 1961; Gohar and Latif, 1961; Mohsin,1962; Bullock, 1967). However, the additionalthin layer of longitudinal muscle fibers presentinside the muscularis in the rectum of thecunner was not reported by these investigators.

AI-Hussaini (1949b) reported that alkalinephosphatase was most abundant in the freeborder of the absorptive cell of three speciesof stomachless minnows-Cypriuus carpio,Gobio gobio, and Riltilus mtilus. Similar re­sults were found along the free border of the

CHAO: DIGESTIVE SYSTEM OF CUNNER

intestinal epithelium of the cunner in cellswhich are in direct contact with the food. Anextremely strong alkaline phosphatase reactionwas found in the intestinal bulb and anteriorhalf of the rectum in the cunner. This reactionseems to be restricted to the free border ofthe epithelial layer of the intestine and rectum.Evidence of active rectal digestion also hasbeen reported by Babkin and Bowie (1928),Ishida (1936), Al-Hussaini (1949b), Bullock(1967), and Western (1971) in other stomach­less fishes.

The close association of the pancreas andbile duct in cunner observed in this studyagrees with the observations of Gohar andLatif (1959) for another labrid, JuUs oygula.Vacuoles (which stained intensively with fastgreen or with aniline blue) were observed inthe supranuclear zone of the columnar epi­thelium of the gallbladder (Figure 17). Noreference to this situation was found in theliterature, and no data were acquired in thisstudy to determine the function of thesevacuoles.

Feeding Habits

Cunners are most active in daytime bothin aquaria and in the field. Their activity de­creased sharply during the night, the fish lyingagainst objects on the bottom or hiding increvices. Torpid behavior was observed duringthe day when the water temperature in theaquarium fell below 4°C. Bigelow and Shroeder(1953) and Green and Farwell (1971) alsonoticed that cunners become torpid duringwinter.

Cunner reach their greatest inshore abun­dance in summer (July- August). They wereabsent from the summer habitat from earlyNovember to late April. Observations made bySCUBA diving indicate that the offshore move­ments began as the water temperature droppedbelow 11 °C (September 1971). A slight migra­tion of cunner during the winter was postulatedby Johansen (1925) and also reported by Bigelowand Schroeder (1953) and Green and Farwell(1971). Local fishermen repOlted the speciesto be present in deeper (more isothermal)waters in the winter. Juveniles tended to move

into shallow water in early spring as reportedby Johansen (1925). Some juveniles were col­lected during this season in brackish water atthe Jackson Laboratory of the University ofNew Hampshire on Great Bay, N.H. This is inaccordance with the statements of Johansen(1925) but is contrary to those of Bigelow andSchroeder (1953).

Cunners fed on both sessile (Mytilus eduUsand Modiol us modiolus) and moving animals(Fuudulus hetfroclitus, GUIiIIiW)'IIS O('fallieus,Nephtys I)//('fm, Nfreis Vil'fllS, and Cembra­tulus la.eteus) in the laboratory and also actedas scavengers, Gut content analyses (Table 1)indicate that cunner are carnivorous ratherthan omnivorous in contrast to statements byJohansen (1925) and Bigelow and Schroeder(1953). There was no evidence that cunneractively consume algae in the aquarium evenwhen starved. Algae found in the gut of cunnerare always small and undigested and are fre­quently associated with digested epiphytic ani­mals (bryozoans, hydrozoans, and larval mol­luscs). A change of prey was noted betweenjuvenile and adult cunner (Table 1). Juvenilesfeed mainly on motile crustaceans in the watercolumn, adults on sessile or sedentary animals.A few large, offshore specimens showed a furtherchange in feeding habits.

In this study almost every adult specimenhad mussel shells in the gut, Mussels My til useduUs and Modiolus modiolus covel' the rockfaces in the feeding habitat from which thecunner were taken. Most of the mussels eatenby cunner were less than 2 years old. Manyother labrids are also mollusk feeders (Suye­hiro, 1942; Al-Hussaini 1947b; Gohar andLatif, 1959). Randall (1967) recorded the foodhabits of 11 species of western Atlantic wrasses-all of which, except for the plankton feedingClcptieus parmi-tended to feed on hard­shelled invertebrates such as mollusks, crusta­ceans, and echinoderms. No algae were men­tioned by these authors except that 5 out of50 specimens of Ha licho(')'es poeciloptfrllshadseaweeds (Viva, etc.) present (Suyehiro, 1942).

Feeding habits of cunner are related to their. jaws, teeth, pharyngeal mill, and also thelength of the intestine as reported for otherstomachless fishes (Suyehiro,1942; Al-Hussaini,

583

1949a; Gohar and Latif, 1961; Mohsin, 1962;Weatherley, 1963). The protrusible jaws ofthe cunner have sharp caninelike teeth whichare adapted to catching, picking, and scrapinganimal foods. The strong muscles (hypobranchialand branchiomeric muscles) associated with themouth can keep the jaws closed tightly, andquick movements of the body could help indetaching sessile organisms from the rocks.The molariform pharyngeal teeth of the cunnerserve as a mill to grind up the hard shells ofthe ingested foods. The probability that well­developed pharyngeal teeth have taken overthe mechanical function of the stomach amongthe stomachless fishes had been suggestedpreviously by Barrington (1942, 1957), Suyehiro(1942), AI-Hussaini (1947b), and Gohar andLatif (1961).

Ingested foods passed rapidly through thebuccal cavity and pharynx in the cunner asin most bony fishes. In the present study, themovement of mussels through the intestineof cunners fed in the laboratory, required 10 to14 hr. Intact and alive mussels were foundin all parts of the gut of freshly killed speci­mens both in the field and aquarium. Some ofthese mussels (less than 16 mm shell length)still were able to resettle. Field observationsindicated that the largest individual mussels(over 100 mm shell length) were scattered onthe surface of bare rocks 5 to 10 m below thetidal zone. However, the major population ofthe mussels formed patches or clusters inthe intertidal zone. Perhaps cunner play arole in the vertical distribution of mussels.

No specific area of food storage was foundin the cunner; the gut of fish which had beenfed all they desired was completely packed withfood, and it appeared that the entire intestinecan serve as a storage organ while digestionis being completed. The intestinal bulb ofstomachless fishes may substitute as a storageorgan (Babkin and Bowie, 1928; Barrington,1942; AI-Hussaini, 1947a; Khanna, 1961;Mohsin, 1962; Bullock, 1967).

Alkaline conditions (pH 7.0-8.5) prevailedthroughout the gut in all specimens of cunnersexamined. In starved controls, there was littlevariation in pH value observed among regions

584

FISHERY BULLETIN: VOL. 71, NO.2

of the intestine. However, in feeding fishes,the pH varied in a random fashion fromregion to region and showed no significantgradient. Phosphatase tests show a positivereaction for alkaline phosphatase, but negativefor acid phosphatase. Intercellular digestionper se in the cunner is exclusively alkaline.Among other stomach less fishes, alkaline diges­tion was observed throughout the gut by Babkinand Bowie (1928), Ishida (1936), Barrington(1942, 1957), AI-Hussaini (1947a), Gohar andLatif (1959, 1961), and Bullock (1967).

Szarski (1956) discussed the advantages ofalkaline digestion in stomachless freshwaterfishes. He referred to the high biological valuein retention of essential ions, which could alsoapply to the present species. Cunners feedmainly on shelled animals and the incidenceof tooth damage is high. As is evident fromhaving developing teeth along the edge of theold ones on the premaxillary, dentary, andpharyngeal bones. The apparent continuousregeneration and growth of teeth needs largeamounts of calcium. The calcium supply can­not be obtained from the calcium carbonateof the animal shells due to the alkaline condi­tion in the gut. Presumably, the calcium sourceis from the calcium pool of the viscera of theingested animals.

ACKNOWLEDGMENTS

I thank my thesis committee members, H. D.Ahlberg, B. B. Collette, C. A. Meszoely, andN. W. Riser of the Biology Department ofNortheastern University. My deepest apprecia­tion goes to N. W. Riser, Marine ScienceInstitute, Northeastern University, for hisencouragement and advice from the very be­ginning to the completion of this researchand to B. B. Collette, Systematics Laboratory,National Marine Fisheries Service, NOAA,for his critical comments and help. In addi­tion, I acknowledge helpfUl comments onthe contents and organization of this paper byR. H. Gibbs, Jr., Division of Fishes, U. S.National Museum, and J. A. Musick andJ. D. McEachran, Virginia Institute of MarineScience.

CHAO: DIGESTIVE SYSTEM OF CUNNER

LITERATURE CITED

AL-HuSSAINI, A. H.1947a. The anatomy and histology of the alimentary

tract of the plankton-feeder, Atherina forskaliRupp. J. Morpho!. 80:251-286.

1947b. The feeding habits and the morphology ofthe alimentary tract of some teleosts living inthe neighbourhood of the Marine Biological Sta­tion, Ghardaqa, Red Sea. Pub!. Mar. Bio!. Stn.AI-Ghardaqa, (Red Sea) 5: 1-61.

1949a. On the functional morphology of the ali­mentary tract of some fish in relation to dif­ferences in their feeding habits: anatomy andhistology. Q. J. Microsc. Sci. 90: 109-139.

1949b. On the functional morphology of the ali­mentary tract of some fish in relation to dif­ferences in their feeding habits: cytology andphysiology. Q. J. Microsc. Sci. 90: 323-354.

1964. On the nature of certain pear-shaped cellsin the intestinal epithelium of fish. Bul!. Inst.Egypte 40:23-32.

BABKIN, B. P., AND D. J. BOWIE.1928. The digestive system and its function in

Fllndllills ""Iaoe/illls. Bio!. Bul!. (Woods Hole)54: 254-277.

BAKER, J. R.1942. The free border of the intestinal epithelial

cell of vertebrates. Q. J. Microsc. Sci. 84:73-103.BARRINGTON, E. J. W.

1942. Gastric digestion in the lower vertebrates.BioI. Rev. (Camb.) 17: 1-27.

1957. The alimentary canal and digestion. InM. E. Brown (editor), The physiology of fishes,Vol. I, p. 109-161. Acad. Press, N.Y.

BIGELOW, H. B., AND W. C. SCHROEDER.1953. Fishes of Ihc Gulf of Maine. U.S. Fish

Wild!. Serv., Fish. Bull. 53, 577 p.BISHOP, c., AND P. H. ODENSE.

1966. Morphology of the digestive tract of the cod,Gadlls II/OrJIlIll. J. Fish. Res. Board Can. 23:1607-1615.

BOLTON, L. L.1933. Basophile (mast) cells in the alimentary

canal of salmonoid fishes. J. Morpho!. 54:549-591.BUCKE, D.

1971. The anatomy and histology of the alimentarytract of the carnivorous fish the pike Esox IlIciusL. J. Fish BioI. 3:421-431.

BULLOCK, W. L.1963. Intestinal histology of some salmonid fishes

with particular reference to the histopathologyof acanthocephalan infections. J. Morpho!. 112:23-44.1967. The intestinal histology of the mosquitofish, Gambusia affinis (Baird and Girard). ActaZoo!. (Stockh.) 48:1-17.

BURNSTOCK, G.1959. The morphology of the gut of the brown

trout (Sa/II/o II"I/I/a). Q. J. Microsc. Sci. 100: 183­198.

CURRY, E.1939. The histology of the digestive tube of the

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