seasonal atrophy of the visceral organs in a sea cucumber

Seasonal atrophy of the visceral organs in a sea cucumber

PETER V. FANKBONER AND J. LANE CAMERON Department of Biological Sciences, Sirnon Fraser University, Burnaby, B. C . , Canada V5A I S6

Received March 4, 1985

FANKBONER, P. V., and J . L. CAMERON. 1985. Seasonal atrophy of the visceral organs in a sea cucumber. Can. J. Zool. 63: 2888-2892.

The gut, gonad, respiratory trees, and circulatory system of the commercial sea cucumber Parastichopus californicus are annually lost as a result of atrophy of these organs and not, as originally supposed, through spontaneous, seasonal evisceration. Visceral loss is preceded by cessation of feeding-locomotory behaviour. Torpor ensues, and the visceral tissues are absorbed through a progressive process which includes phagocytosis by the sea cucumber's coelomocytes and, in some instances, the scavenging activities of endosymbionts. Regeneration of the viscera occurs within several weeks. Similar seasonal atrophy of the visceral organs has not been reported to occur in other coelomate organisms. We hypothesize that visceral atrophy in P. californicus is an expression of seasonal diapause induced by reduced food availability.

FANKBONER, P. V., and J. L. CAMERON. 1985. Seasonal atrophy of the visceral organs in a sea cucumber. Can. J. Zool. 63: 2888 - 2892.

Le tube digestif, les gonades, les organes arborescents et le systeme circulatoire du concombre de mer commercial Parastic-hopus californicus sont perdus chaque annke par atrophie et non, comme on I'a gknkralement suppod, par kvisckration spontanke saisonniere. La perte des visceres est prkckdke par la cessation des comportements locomoteurs et alimentaires. Ce phknomene est suivi par une griode de torpeur et les tissus visckraux sont absorbks par u n processus progressif au cours duquel il se fait de la phagocytose par les coelomocytes et, parfois aussi, par I'activitk dktritivore d'endosymbiontes. La regk- nkrescence des visceres se fait apres plusieurs semaines. Une telle atrophie saisonniere des organes visckraux n'a jamais kt6 signalke chez d'autres coelomates. Nous croyons que I'atrophie des visceres chez P. californicus est la manifestation d'une diapause saisonniere dkclenchke par la rkduction de la nourriture disponible.

[Traduit par le journal]

Introduction Brachial autotomy is a characteristic behaviour of many

echinoderms, but sea cucumbers, which lack arms, possess the remarkable ability to cast free and forcefully expel their gut, gonad, and respiratory trees (Barnes 1980; Clark 1977; Emson and Wilkie 1980; Hyman 1955; Swan 1966). Evis- ceration behaviour has been well documented for nearly a cen- tury, and many workers have viewed visceral autotomy as a superb "natural" preparation for following the processes of lost tissue regeneration (Bai 197 1 ; Bertolini 1933; Dawbin 1949; Domantay 1931; Minchin 1892; Mosher 1956, 1965; Scott 19 14; Tracey 1972). In this regard, several methods have been contrived to rapidly induce evisceration in sea cucumbers including rough handling, elevation of body temperature, injec- tions of strychnine or ammonia water, and electric shock (Bertolini 1932, 1933; Dawbin 1949; Kille 193 1 , 1935; Pearse 1909; Smith and Greenberg 1973). Direct observations of visceral autotomy in situ are lacking, but ejected viscera are believed to function as a decoy to retain the interest of an attacking predator until the eviscerated sea cucumber can safely crawl from the scene (Mottet 1976; cf. Emson and Wilkie 1980). Viscera lost in this manner are quickly regenerated by the holothurian, a modest recompense for survival.

It has been suggested that whole populations of the commercial sea cucumber Parastichopus californicus may participate in seasonal mass eviscerations (Clark 1977; Swan 196 1). For instance, of the 81 specimens of P . californicus that Swan (1961 ) collected by potato hook or dredge at Friday Harbor, Washington, during the fall of 1959, 49 individuals possessed incomplete visceral organs. During the winter months, however, all of the 70 specimens that he examined contained normal and complete viscera. Thus, Swan believed that P . califor-

nicus had undergone spontaneous seasonal evisceration. Over a 3-year period, we have reexamined Swan's hypothe-

sis of annual mass spontaneous evisceration and agree that there is a seasonal absence of the viscera in P. californicus. To the contrary, however, we suggest that this sea cucumber does not lose its coelomic organs as a consequence of self-evisceration, but rather as the outcome of an orderly, progressive process of visceral atrophy.

Methods Adult specimens (430) of Parastichopus californicus were collected

over a 40-month period (Fig. I ) by scuba diving in subtidal waters (depth 3-20 m) at Woodlands Bay, Indian Arm Fjord, British Columbia. Because of the delicate condition of P. californicus during the autumnal months, during collection, sea cucumbers were care- fully eased into plastic bags containing an appropriate volume of seawater. Immature sea cucumbers ( 5 4 years old and numbering over 200) were collected concurrently to establish whether state of sexual maturity was related to seasonal evisceration. To confirm that this sampling was representative, we also examined all age groups of P. californicus (P. V. Fankboner and J. L. Cameron') obtained under similar conditions at Kelvin Grove, and Croker Island in British Columbia, and adjacent to Friday Harbor Laboratories, San Juan Island, Washington State. Collection of all adult and most immature sea cucumbers was accomplished using random selection techniques. However, primarily because of their cryptic habits, immature sea cucumbers (12.5 cm), or juveniles, were collected as we could find them by intensive searching of collection sites.

Each sea cucumber was dissected within several hours of collection to establish both the condition of the viscera and the presence of endosymbionts within the gut and coelomic cavity. Following dis- section, most of these animals were stripped of viscera (if present) and wet-weighed to detect seasonal changes, if any, in growth rate of the body wall.

'Fankboner, P. V., and J. L. Cameron. Dynamics of growth in the Results

commercial sea cucumber Parastichopus californicus (Stimvson). Dissections of P . californicus revealed that visceral atrophy . a .

Manuscript in preparation. (Fig. 1) is essentially autumnal, but can occur from late ~ u l y to

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FANKBONER A N D CAMERON 2889

Visceral Condition

FIG. 1 . Seasonal atrophy of the visceral organs in P. c.cl1iJornicu.s collected over a 40-month period at Woodlands Bay, Indian Arm Fjord, British Columbia. Conditions of the viscera represented in this figure include complete n, degenerating D, and regenerating m. The total number of sea cucumbers examined was 430, with each monthly sample of 2 10 individuals taken by random sampling techniques.

March. Typically, the catabolic process begins in September with P. californicus ceasing to fill its gut with food and dis- playing soporific behaviour. At the onset of atrophy, feeding and locomotory movements cease, the anterior quarter of the sea cucumber is elevated just off the substratum, and the feeding tentacles lie almost completely withdrawn within the oral hood. Tube foot contact with the substratum is partially reduced at this time, and the sea cucumbers are somewhat easier to dislodge. While the sea cucumber is in this state of torpor, it does not respond to the delicate probing which under normal circumstances would cause P. californicus to move away by crawling or twisting. Surprisingly, while P. californicus is unresponsive to probing during torpor, it is hypersensitive to handling or jostling and is prone to spew out its partially atro- phied viscera should reasonable care not be taken in the course of collection. Handling does not normally produce evisceration behaviour in P. californicus outside the period of visceral atrophy.

Within the coelomic cavity of P. californicus, the looped, alimentary canal is the central visceral organ. It is suspended within the coelomic fluid by the dorsal mesentery and gives support to several organ systems including the gonad basis, the respiratory trees, and the circulatory system or "rete mirabile". The gonad basis is a saddle-shaped organ attached to the outer, dorsalmost wall of the pharyngeal bulb and when P. californicus is reproductively "ripe" this structure gives rise to numerous spaghettilike tubes containing gametes. Paired respiratory trees (water lungs) arise from a short single trunk connected antero-dorsally to the entrance of the large intestine at the cloaca. The rete mirabile comprises a delicate network of ves- sels which is histologically contiguous with the gut and more loosely invests the paired respiratory trees. During visceral atrophy, these organs undergo more or less complete reduction to minute swellings or nodules of tissue primordia. It is inter- esting to note, however, that reduction of the gut tube excludes those terminal segments which support the gonad saddle and respiratory trees.

As gut degeneration progresses, the intestine contracts both in length and diameter until it is reduced to a straight, firm, pencil lead thick tube running along the margin of its mesentery. The gut tube's colour shifts from a cream - pale tan colour to medium brown during this initial stage of atrophy. The gut tube continues to shrink reaching a final stage where

it becomes reduced to a thin line of white, translucent, primor- dial tissue on the mesentery margin.

The gonad, circulatory system, and respiratory trees undergo resorption and reduction in size similar to that described for the gut. The gonadal tubules, however, often disintegrate into short lengths following the onset of atrophy and are further rendered by phagocytic coelomocytes and (or) ejected from the coelomic cavity through minute, ciliated cloacal ducts.

Both free and aggregated (brown bodies) phagocytic coelomocytes were associated with resorption of coelomic visceral tissues. Pieces of tissue, believed to be of visceral origin, and eggs of the flatworm Anoplodium hymanae were found within free coelomocytes and (or) brown bodies. The latter have been observed emerging from the outer cloacal wall via minute ciliated ducts communicating between the coelom and cloacal chamber (personal communication from Dr. George L. Shinn of Friday Harbor Laboratories, University of Washing- ton). The degree to which coelomic blood cells participate in visceral atrophy remains to be established (see Hetzel (1963, 1965) regarding the role of coelomocytes in P. californicus).

Visceral resorption in all symbiont-infested sea cucumbers was accompanied by the feeding activities of scavenger proto- zoan and platyhelminth endosymbionts living within the coelomic cavity. Cream-coloured blisters ( 1 -8 mm) are a characteristic feature of the visceral surfaces during the final stages of atrophy; these bodies contain masses of sporocysts from eugregarine protozoans. Blisters are reduced or absent in preatrophied sea cucumbers. Umagillid turbellarians are also conspicuously numerous during visceral atrophy in P. californicus and obtain nutriments from feeding on the sea cucumber's gut tissues (Ozametra sp.) or from the coelomic fluid (A. hymanae) .

The presence of endosymbionts does not appear obligatory to the process of visceral atrophy. In the majority of P. californicus examined, the infestation level during visceral atrophy as evidenced by adult flatworms and (or) sporozoan blisters was similar to that seen in preatrophy coelomic cav- ities. There was an obvious difference in the clarity of coelomic fluid in preatrophied sea cucumbers and those undergoing visceral resorption; in the latter, the coelomic Iluid was remark- ably cloudy as a result of the presence of cellular debris and microorganisms.

Within 2 to 4 weeks following visceral loss, the visceral stem

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2890 C A N J ZOOL. V O L h i . 19x5

500 1 In addition, the pol ypide dies during regression resulting in

FIG. 2. Mean body weight (tentacle crown. body wall, and longi- tudinal muscle band complex less the coelomic contents) of P. c~111ti)r- nicus taken from the population samples shown in Fig. I . The maximum mean body weight observed during the preatrophy period was significantly larger than that reported during the time of visceral regeneration (by ANOVA, P < 0.01 ). The curve was fitted by computer.

tissues of P. I-oljfornic-us regenerate new, more or less completely differentiated coelomic organs. The gut tube is the first visceral organ to regenerate. I t begins as a fairly uniform thick- ening of the tissue primordia, followed by lumen formation at the anterior and posterior ends; these migrate towards the central portion of the regenerating gut until they meet. The walls of the new gut are nearly transparent, and just before re- sumption of feeding behaviour, the anterior portion of the tube contains a clear brown fluid. Feeding may begin following completion of a continuous gut lumen. Next. the respiratory trees and circulatory system differentiate and the gonad begins to regrow its branched tubules. The latter organ does not reach complete development until just before spawning during the summer months. Sea cucumbers that have not reached reproductive age ( 5 4 years old) demonstrate the same pattern of seasonal visceral atrophy as the adults except, of course, the gonad is not involved.

Body wall weight in P. c.ul1fornicu.s (Fig. 2) follows an annual cycle which reaches its lowest ebb early in the year at about the commencement of visceral regeneration and its high- est level in early fall when visceral degeneration begins. Shrinkage of the body wall during the atrophy period may exceed 25% of its maximum preatrophy value. Sea cucumbers recover preatrophy size and weight in their body wall during the spring and summer months when normal feeding patterns emerge.

Discussion Annual resorption and regeneration of the gut, respiratory

organs, circulatory system, and gonad per se, which we have observed in Parastichopus c.ullfornic-us, have not been reported to occur in other solitary, coelomate organisms. The nearest parallel condition can be found in the Bryozoans (Ectoprocta) in which cyclic polypide regression and renewal is a characteristic feature. However, unlike the seasonal periodicity found in visceral atrophy, bryozoan regression may occur at any lime when the waste accumulation in the polypide's gut tissue reaches levels which prevent efficient absorption of nutrients.

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virtually the whole organism degenerating into a conspicuous brown body (Gordon 1977).

Within the holothuroidea, seasonal visceral atrophy may not be exclusive to the California sea cucumber. There are indi- cations in the literature that this bizarre process may have been previously observed in other holothurian species, but because of incomplete information or possibly misinterpretation of observations, instances of seasonal visceral atrophy in aspidochirotid (and perhaps dendrochirotid) sea cucumbers have gone unreported.

One case in point is the commercially harvested and exhaus- t ivel y studied West Pacific sea cucumber, Stichopus juponicus. Tanaka (39586) notes autumnal periods of aestivation for S . jerponicu~ during which time the gonad is always " . . . small in size, showing resting stage." He adds that growth of the gonad begins following the renewal of feeding behaviour in Noven-her. "Resting" in S. jcrponicus is also manifested by shrinking of the body and loss of weight; during this period, the intestine, which is normally 5.7-6.4 times the length of the body, is shorter than the body length (Suguri 1965). At the cel l~~lar level, regenerative histogenesis of the gut epithelium in S . juponicu.~ has been described by Leibson (1982) who observed a profound morphofunctional rearrangement of the intestine resulting in renovation of the sea cucumber's digestive tract. Several additional findings of intestinal shrinkage in S . jcrpor1ic.u.s appear in the literature (Mitsukuri 1903; Tokuhisa 19 15; Tanaka 1958cr). The latter observations are anecdotal and not based upon quantitative data, but they do contribute to the accumulating evidence indicating that S . jcrponicus may also undergo autumnal visceral loss similar to that reported here for P. I-a1fornicu.s.

Less direct references to possible seasonal atrophy of the visceral organs in sea cucumbers include studies on the aspi- dochirotids Actinop~gcr crgassizi (Mosher 1965). Holothurid floridancr (Emson and Wilkie 1980), Holothuria tubulosa (Bertolini 1930), Pcrrcrstichopus pcrrvimcn.sis ( Y ingst 1982) Stichopus regalis (Bertolini 1933), and Stichopus tremulus (Jespersen and Liitzen 197 1 ), and the dendrochirotids Cucum- aria 1lrbric.u (Engstrom 1982), Aslia lyfevrei (Costelloe and Keegan 1984), Eupc)ntcrctcr yuinyuesc~mita (Byrne 1983), and Lc>ptopc>ntcrctcr elongcrta (Fish 1967). The foregoing species either have been observed undergoing seasonal torpor and (or) have large numbers of their population missing viscera during predictable annual periods.

While our findings establish that seasonal visceral atrophy occurs in P. ~-al~fornicus and may be responsible for observed visceral absence in other aspidochirotid sea cucumbers, spontaneous evisceration may account for visceral loss in the dendrochirotid Eupentcrc.tu quinyuesemita. For instance, Byrne ( 1985) collected E. yuinyue.semitu during scuba dives between November 198 1 and March 1983 off Ten Mile Point, Victoria, B.C., and during one of her dives found 7 specimens in the process of evisceration and the rotting viscera from 20 animals at the study site. She states that these E. yuinyuesemitu were "particularly abundant" in comparison to noneviscerating holothurians and believes that her observations establish the first proof of seasonal visceral autotomy in a sea cucumber. We are confused, however, by inconsistencies between these data (Byrne 1985), their original source (Byrne 1983), and their interpretation by the author. For this same dive of discovery, Byrne (1983) reports "autotomized viscera strewn across the substrate" (she provides no numbers, but we presume she refers

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F A N K B ~ N E R A N D C A M E R ~ N 289 1

to viscera from the 20 animals noted above) in a sampling area where the mean population density of E. quinque.srmitu was 780/m2 (Byrne 1985). We can assume that Byrne's observations could not avoid taking in a benthic area of at least several square meters; thus, we fail to see justification for her evaluations of high frequency of visceral autotomy and the suggestion of wide distribution of ejected viscera by a number of animals representing less than 1% of the sampled population. Byrne (1983, 1985) has not observed in sitir the stimulus for visceral autotorny in E. quinquc~srmi tc~; yet, while noting the presence of the predator sea stars Soluster- s t impsoni and Drrmustrr ius imbricutu in the evisceration area, Byrne ( 1985) seizes upon spontaneous evisceration in preference to predation by sea stars as explanation for the lost viscera. I t is evident that Byrne (1985) has failed to evaluate her data in a rigorous and unbiased manner. Thus, in our view, whether spontaneous evisceration causes seasonal visceral loss in sea cucumbers still remains to be established.

The term diapause describes a period of physiologically enforced dormancy in an organism between periods of activity, and may be precipitated by photoperiod, temperature, mois- ture, or nutrient availability (Lees 1955; Chapman 197 1 ; Braune 1973; Waldbauer 1978; Hodek 1983). We suggest that seasonal visceral atrophy in P . c.allforni~.u.s falls sufficiently within these terms of reference to be categorized as a form of diapause. Dormancy in P . 1~c11iji)rni~~u.s is clearly physiologically enforced and includes the autumnal weeks during which feeding and locomotion cease, the sea cucumber dis- plays a state of torpor, and seasonal visceral atrophy occurs. Following regeneration of the gut, normal feeding and locomotory behaviour ensues. An intriguing question regarding diapause in P . ~ w l i f o r n i ~ ~ u s is its causation.

There are no clear data, to date, suggesting how and why this extraordinary physiological process &curs in P . c.alifornicus and, probably, in other aspidochirote holothurians reported to have spontaneous autumnal evisceration (Bertol ini 1 932; Swan 1961 , 1966; Jespersen and Lutzen 197 1 : Lutzen 1979). Sea- sonal diapause in P . 1.n1ifornic.u~~ does not appear to be linked with reproduction because its onset precedes sexual maturation by 3-4 years. Costelloe and Keegan ( 1984) hypothesize that seasonal torpor in the dendrochirotid Asl ic~ Ic<fkvr~i may be cued by a decrease in water temperature, associated with seasonal turbulent conditions and the energy budget of feeding. Sea temperatures at depths inhabited by P . 1w1~fornicu.s in Indian Arm Fjord (subtidal to 25 m) range over the year between 4 and 9°C (Gilmartin 1962), but this represents a relatively modest seasonal change compared with most coastal waters (Sverdrup e t a l . 1942); thus, we believe temperature is unlikely to be a direct factor effecting diapause in P . c~a1jforni~~ir.s. Pearse and Eernisse (1982) have demonstrated that day length controls reproduction in the intertidal sea star Pi.scist~r ochrc~cr irs . In our collection sites, we have never found P . ~ ~ m l ~ f o r n i ~ . i ~ s living deeper than 25 m. Thus, it is possible that sunlight regulates reproductive cycling in P . cul i forni~~u.s and may intluence the onset of diapause as well.

We are currently testing both photoperiod and nutritional availability as potential factors synchronizing seasonal diapause in P . c.alifornic.us. However, physiological and behav- ioural evidence to date indicates that food availability may be the more promising causal factor of the two. For instance, in Gilmartin's ( 1964) data on net primary production for lndian Arm Fjord, he observed that the summer plankton bloom for these waters effectively ends in August, a period which closely

precedes normal autumnal diapause in P . 1~c11jfornicu.s. More- over, whenever actively feeding P . 1~a1~fi)rnicir.s are collected and transferred to aquaria lacking detritus or surface algae, they abruptly cease most locomotory -feeding activity. If deprived of food for several days to a week, they enter a state of torpor indistinguishable from that characteristic of seasonal diapause. Further in this regard. several specimens collected during the summer months and kept in the absence of food underwent visceral atrophy in captivity about 60 days hc<fi)rc) their cohorts in the field. Finally, loss of about 25% of the body-wall weight during diapause may also support the concept of a nutritional factor regulating torpor and eventual visceral atrophy in P . ~*allforniclr ,s . All or a portion of this evidence, however, may be circumstantial, and we are treating it with caution until our hypothesis is verified or negated by controlled experimen- tation. Seasonal diapause is a new and exciting area in the physiology of echinoderms that begs further investigation.

Acknowledgments We thank Jack da Silva, Bruce Leighton, and Tim Smith for

assistance in the collection of sea cucumbers. Tim was also the first of us to notice shrinking of the gut tube in Pure~.st i~~hopu.s I-c~ljfornic.u,s and thus he got us started on the whole issue of spontaneous evisceration versus seasonal visceral atrophy. Operational monies from the Science Council of British Col- umbia and the Natural Sciences and Engineering Research Council of Canada are much appreciated. We are also grateful to Friday Harbor Laboratories, University of Washington, for providing facilities.

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