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THE CROWDING EFFECT REVISITEDAuthor(s) Larry S RobertsSource Journal of Parasitology 86(2)209-211 2000Published By American Society of ParasitologistsDOI httpdxdoiorg1016450022-3395(2000)086[0209TCER]20CO2URL httpwwwbiooneorgdoifull1016450022-3395282000290865B02093ATCER5D20CO3B2

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209

J Parasitol 86(2) 2000 p 209ndash211q American Society of Parasitologists 2000

THE CROWDING EFFECT REVISITED

Larry S RobertsdaggerDepartment of Biology University of Miami Coral Gables Florida 33124

Much has been learned of the biology of cestodes since ClarkRead published his paper in 1951 yet in many respects ourknowledge remains distressingly meager Read observed thatin Hymenolepis diminuta and several other species the sizeattained by the worms in their definitive host was roughly in-versely proportional to the number of worms present a phe-nomenon he called the lsquolsquocrowding effectrsquorsquo The adaptive valueof the crowding effect seems self-evident the size of the indi-vidual worms is limited by whatever means to an aggregatemass that the host can tolerate without adverse consequencesThe known list of cestodes that demonstrate a crowding effecthas increased little in the past 40 yr and a definitive explanationfor the effectrsquos mechanism of operation remains elusive Inas-much as development and growth of the worms is being con-trolled by some means external to the individuals in the popu-lation the mechanism of this control is of considerable biolog-ical interest

In their accompanying paper Bush and Lotz (1999) point outthat ecological consideration of crowding can relate to preda-torndashprey relationships or to competition Because we can dis-regard predatorndashprey relationships I focus here on competitionwhich in turn can take the form of exploitative competition(required resources reduced in supply by the organisms) or in-terference competition (substances released by organisms hav-ing an adverse effect on others in the population) I also ex-amine the possible role of the host immune response in thecrowding effect

Exploitative competition

Investigations for the next 25ndash30 yr after Readrsquos paper (Read1951) assumed that the mechanism was exploitative in formIn that paper he suggested that oxygen might be the requiredresource and that the resource was lsquolsquoprobably not a food sub-stance obtained from the foodstuffs ingested by the hostrsquorsquo Ad-ditional investigation by Read and his coworkers showed un-equivocally that quantity and quality of host dietary carbohy-drate did indeed affect worm growth (Read 1959) He con-cluded that cestodes require carbohydrate for growth andreproduction that the carbohydrate is obtained from host in-gesta and that lsquolsquo[t]he crowding effect in cestode infections maybe interpreted in terms of competition for utilizable carbohy-drate by the individual worms in the populationsrsquorsquo

Roberts (1961) reported that the earliest manifestations of thecrowding effect could be detected already at 8 days postinfec-tion an age at which the worms were only 002ndash015 the massthey attained when mature (17 days postinfection) He alsofound that proglottid production was inhibited by crowdingwhich implied that cells in the tiny zone immediately following

Invited Review to complement C P Read 1951 The lsquolsquocrowdingeffectrsquorsquo in tapeworm infections Journal of Parasitology 37 174ndash178

dagger Address for correspondence 27700 SW 164 Ave Homestead Florida33031

the scolex were inhibited in their differentiation of new pro-glottids a lsquolsquopoint effectrsquorsquo Glycogen stores were inversely af-fected by increased worms present Proportionately greater lipidaccumulation was correlated with increased crowding Roberts(1966) found that host diets that were suboptimal in carbohy-drate quality or quantity did indeed inhibit proglottid productionand result in lower glycogen and higher lipid in crowdedworms Although those observations supported Readrsquos hypoth-esis just how carbohydrate limitation could inhibit wormgrowth at 8 days postinfection yet be sufficient to support amass of tapeworms 10ndash50 times greater at 17 days was unex-plained In fact evidence suggests that 8-day-old worms cancompete more effectively (if there is competition) for glucosethan can mature worms (Starling 1975 Henderson 1977 Rob-erts 1980) and Henderson (1977) reported that 8ndash10-day-oldcrowded worms showed lower rates of glucose absorption thanuncrowded ones Therefore if competition for host dietary car-bohydrate is part of the mechanism of the crowding effect itprobably operates later rather than earlier in worm develop-ment perhaps after absorption sites for glucose have been mod-ulated by some other signal It is certainly possible that 1 mech-anism predominates when the worms are 8 days old and anotherat 17 days

The hypothesis that mature worms might compete for car-bohydrate was supported by Mead and Roberts (1972) whostudied starch digestion and absorption in the rat small intestineBased on that study plus measurements of the amount of starchin the normal diet of the rats and estimates based on in vitroglucose consumption by H diminuta lsquolsquocompetition among theworms for glucose is quite plausiblersquorsquo (Mead and Roberts1972) when the mass of worms in the hostrsquos intestine approach-es its maximum The observation that a larger proportion of theenzyme glycogen synthase is in its active I form in crowdedworms compared to that in uncrowded worms may be anotherindication of competition for carbohydrate (Dendinger and Rob-erts 1977)

A few other candidates for limiting resources have been in-vestigated Despite the consumption of oxygen by cestodeswhen oxygen is available no effect of oxygen presence or con-centration on in vitro development of H diminuta was detectedby Roberts and Mong (1969) thus Readrsquos (1951) original hy-pothesis was rendered highly unlikely Also unlikely was com-petition for a vitamin in the host diet because prevention ofcoprophagy was necessary to demonstrate a requirement by Hdiminuta for any vitamin (pyridoxine) in the host diet (Platzerand Roberts 1969) Interestingly a diet deficient in riboflavinresulted in worms larger than controls whether or not coproph-agy was prevented (Platzer and Roberts 1970)

Interference competition

Roberts (1961) suggested that some compound(s) excretedby the worms could adversely affect growth of other worms inthe population When crowded worms were recovered from the

210 THE JOURNAL OF PARASITOLOGY VOL 86 NO 2 APRIL 2000

host and incubated in a balanced salt solution synthesis ofDNA RNA and protein were all significantly lower than incomparable uncrowded worms (Bolla and Roberts 1971) Aworm-conditioned saline (WCS) was prepared by incubatingcestodes for 12 hr in a balanced buffered salt solution withadded glucose and antibiotics (Insler and Roberts 1980) In-corporation of 3H-thymidine into DNA of freshly recovered 10-day-old H diminuta was inhibited by incubation in the WCS(glucose replenished) compared with controls incubated in freshsaline WCS prepared with more crowded worms producedgreater inhibition (Roberts and Insler 1982) That this in factrepresented DNA synthesis was indicated by the observationsthat thymidine uptake was not inhibited by WCS that absorbedthymidine was rapidly incorporated into DNA and that the un-incorporated pool of thymidine in the worms was negligible(Davis 1982)

Of the many compounds released by H diminuta during invitro incubation the following accounted for most if not allof the inhibitory properties of WCS succinate acetate glucos-aminic acid and cGMP (Insler and Roberts 1980 Zavras andRoberts 1984 1985) Cook and Roberts (1991) tested the ef-fects of these substances on growth of H diminuta in vivoThey infected rats with H diminuta implanted an intestinalcannula at 7 days postinfection and perfused the intestine witha solution containing the putative crowding factors for 7 daysat 50 ml per day then they recovered the worms Controls wereperfused with 50 ml of water Experimental worms were 53smaller than controls and had fewer proglottids but the 2groups did not differ in carbohydrate concentration Thusgrowth and proglottid production had been inhibited indepen-dent of dietary carbohydrate or competition for carbohydratein vivo in the artificial presence of natural products the wormsare known to secrete If Moniliformis moniliformis producesand is sensitive to the same products it might explain the re-duction in weight of both worms in concurrent infections withH diminuta (Holmes 1961) That question awaits investigation

Myoelectric changes caused by H diminuta in the small in-testine of rats have been reported (Dwinell et al 1994 19951998) altering intestinal motility such that contractility is in-creased and propulsion is decreased The myoelectric alter-ations could be detected first at 8 days postinfection and dis-appeared within 24 hr after the worms were removed by praz-iquantel The alterations were induced in tapeworm-naive ratsby administration directly into the intestine of worm homog-enates or tegument-enriched fractions Whether the myoelectricalterations have any relationship to the crowding effect is amatter for conjecture at present but their concurrence in timeduring worm development is at least a remarkable coinci-dence It is possible that decreased propulsion slows intestinaltransit increasing the length of time that worms are surroundedby nutrients from the host meal

Host immune response

Our knowledge of the host immune response against adultcestodes especially H diminuta has been reviewed recently(Andreassen et al 1999) and those findings need not be sum-marized in detail here Contrary to opinion prevalent 40 yr agoit is now clear that H diminuta stimulates an immune responseresulting in antibody production and intestinal inflammatory re-

action Immune phenomena can be demonstrated most easilywith H diminuta in mice but effects in rats are more subtlepresumably resulting from the long coevolution of rat and tape-worm Effects appear to vary with rat strain feeding regimeage and with worm strain (Andreassen et al 1999) Interest-ingly no crowding effect was observed either in the tapewormsor the acanthocephalans in hamsters infected concurrently withH diminuta and M moniliformis (Holmes 1962)

Destrobilation and expulsion most commonly when someworms in a crowded infection are expelled are attributed tohost immune response Such phenomena usually have been ob-served in chronic infections ie from a few to many weekspostinfection Hopkins and Andreassen (1991) reported thatwhen H diminuta in a rat were expelled chemotherapeuticallyand the hosts were reinfected at various times thereafter growthof the secondary worms was inhibited The depressive effectwaned rapidly during the first few weeks after the primary in-fection was expelled but it could still be detected as long as17 mo later They argued that if the host immune responseinhibited growth of secondary worms then the primary wormswould have been subjected to the same conditions and that adynamic equilibrium would be reached between the immuneresponse in the gut and the mass of cestode tissue They be-lieved that reaching that equilibrium not a crowding effectlimited the size of the worms to a level compatible with hostsurvival

Conclusion

In their review Andreassen et al (1999) state several timesthat the crowding effect is due to the host inflammatory re-sponse and that lsquolsquoit is clearly not due to competition for car-bohydrate rsquorsquo Yet at another point in the review they saylsquolsquoThe cause of these reactions between adult tapeworms [iethe inverse relationship between number of worms present andworm size] is probably a combination of intraspecific compe-tition for space and food secretion by the worms of so-calledlsquocrowding substancesrsquo and host immune reactionsrsquorsquo Based onobservations summarized in the present paper we can concludethe following (1) Competition among the worms for availablehost dietary carbohydrate at least when the cestodes approachmaximum size is compatible both with our best estimates ofglucose available to the worms in hosts fed normal diets andwith analyses of worms from hosts fed carbohydrate-deficientdiets (2) Some compounds secreted by the worms in vitro in-hibit DNA synthesis and inhibit growth of the worms in vivomimicking a crowding effect (3) Under certain circumstancesinflammatory reactions in the host gut can inhibit growth of thetapeworms One of the foregoing or some combination thereofprobably explains the crowding effect Clarification of the op-erational mechanism at the molecular level would be of greatinterest

LITERATURE CITED

ANDREASSEN J E M BENNET-JENKINS AND C BRYANT 1999 Immu-nology and biochemistry of Hymenolepis diminuta In Advances inparasitology Vol 42 J R Baker R Muller and D Rollinson(eds) Academic Press London p 223ndash275

BOLLA R I AND L S ROBERTS 1971 Developmental physiology ofcestodes X The effect of crowding on carbohydrate levels and on

ROBERTSmdashTHE CROWDING EFFECT REVISITED 211

RNA DNA and protein synthesis in Hymenolepis diminuta Com-parative Biochemistry and Physiology 40A 777ndash787

BUSH A O AND J M LOTZ 1999 The ecology of lsquolsquocrowdingrsquorsquo Jour-nal of Parasitology 86 212ndash213

DAVIS R E 1982 Nucleotide metabolism in the rat tapeworm Hy-menolepis diminuta PhD Thesis University of MassachusettsAmherst Massachusetts 170 p

DENDINGER J E AND L S ROBERTS 1977 Glycogen synthase in therat tapeworm Hymenolepis diminutamdashI Enzyme activity duringdevelopment and with crowding Comparative Biochemistry andPhysiology 58B 215ndash219

DWINELL M B P BASS AND J A OAKS 1994 Intestinal myoelectricalterations in rats chronically infected with the tapeworm Hyme-nolepis diminuta American Journal of Physiology 267 G851ndashG858

AND 1995 Praziquantel treatment normalizesintestinal myoelectric alterations associated with Hymenolepis dim-inuta-infected rats Journal of Parasitology 81 979ndash984

AND 1998 Hymenolepis diminuta fractionsbut not previous tapeworm infection stimulate intestinal myoelec-tric alterations in vivo in the rat Journal of Parasitology 84 673ndash680

HENDERSON D 1977 The effect of worm age weight and number inthe infection on absorption of glucose by Hymenolepis diminutaParasitology 75 277ndash284

HOLMES J C 1961 Effects of concurrent infections on Hymenolepisdiminuta (Cestoda) and Moniliformis dubius (Acanthocephala) IGeneral effects and comparison with crowding Journal of Parasi-tology 47 209ndash216

1962 Effects of concurrent infections on Hymenolepis dimi-nuta and Moniliformis dubius (Acanthocephala) III Effects inhamsters Journal of Parasitology 48 97ndash100

HOPKINS C A AND J ANDREASSEN 1991 Inhibition of growth of atapeworm Hymenolepis diminuta in its normal host (rat) Interna-tional Journal for Parasitology 21 47ndash55

INSLER G D AND L S ROBERTS 1980 Developmental physiology of

cestodes XVI Effects of certain excretory products on incorpora-tion of 3H-thymidine into DNA of Hymenolepis diminuta Journalof Experimental Zoology 211 55ndash61

MEAD R W AND L S ROBERTS 1972 Intestinal digestion and ab-sorption of starch in the intact rat Effects of cestode (Hymenolepisdiminuta) infection Comparative Biochemistry and Physiology41A 749ndash760

PLATZER E G AND L S ROBERTS 1969 Developmental physiologyof cestodes V Effects of vitamin deficient diets and host coproph-agy prevention on development of Hymenolepis diminuta Journalof Parasitology 55 1143ndash1152

AND 1970 Developmental physiology of cestodes VIEffect of host riboflavin deficiency on Hymenolepis diminuta Ex-perimental Parasitology 28 393ndash398

READ C P 1951 The lsquolsquocrowding effectrsquorsquo in tapeworm infections Jour-nal of Parasitology 37 174ndash178

1959 The role of carbohydrates in the biology of cestodesVIII Some conclusions and hypotheses Experimental Parasitology8 365ndash382

ROBERTS L S 1961 The influence of population density on patternsand physiology of growth in Hymenolepis diminuta (Cestoda Cy-clophyllidea) in the definitive host Experimental Parasitology 11332ndash371

1966 Developmental physiology of cestodes I Host dietarycarbohydrate and the lsquolsquocrowding effectrsquorsquo in Hymenolepis diminutaExperimental Parasitology 18 305ndash310

1980 Development of Hymenolepis diminuta in its definitivehost In Biology of the tapeworm Hymenolepis diminuta H P Arai(ed) Academic Press New York p 357ndash423

AND F N MONG 1069 Developmental physiology of cestodesIV In vitro development of Hymenolepis diminuta in presence andabsence of oxygen Experimental Parasitology 26 166ndash174

STARLING J A 1975 Tegumental carbohydrate transport in intestinalhelminths Correlation between mechanisms of membrane transportand the biochemical environment of absorptive surfaces Transac-tions of the American Microscopical Society 94 508ndash523

210 THE JOURNAL OF PARASITOLOGY VOL 86 NO 2 APRIL 2000

host and incubated in a balanced salt solution synthesis ofDNA RNA and protein were all significantly lower than incomparable uncrowded worms (Bolla and Roberts 1971) Aworm-conditioned saline (WCS) was prepared by incubatingcestodes for 12 hr in a balanced buffered salt solution withadded glucose and antibiotics (Insler and Roberts 1980) In-corporation of 3H-thymidine into DNA of freshly recovered 10-day-old H diminuta was inhibited by incubation in the WCS(glucose replenished) compared with controls incubated in freshsaline WCS prepared with more crowded worms producedgreater inhibition (Roberts and Insler 1982) That this in factrepresented DNA synthesis was indicated by the observationsthat thymidine uptake was not inhibited by WCS that absorbedthymidine was rapidly incorporated into DNA and that the un-incorporated pool of thymidine in the worms was negligible(Davis 1982)

Of the many compounds released by H diminuta during invitro incubation the following accounted for most if not allof the inhibitory properties of WCS succinate acetate glucos-aminic acid and cGMP (Insler and Roberts 1980 Zavras andRoberts 1984 1985) Cook and Roberts (1991) tested the ef-fects of these substances on growth of H diminuta in vivoThey infected rats with H diminuta implanted an intestinalcannula at 7 days postinfection and perfused the intestine witha solution containing the putative crowding factors for 7 daysat 50 ml per day then they recovered the worms Controls wereperfused with 50 ml of water Experimental worms were 53smaller than controls and had fewer proglottids but the 2groups did not differ in carbohydrate concentration Thusgrowth and proglottid production had been inhibited indepen-dent of dietary carbohydrate or competition for carbohydratein vivo in the artificial presence of natural products the wormsare known to secrete If Moniliformis moniliformis producesand is sensitive to the same products it might explain the re-duction in weight of both worms in concurrent infections withH diminuta (Holmes 1961) That question awaits investigation

Myoelectric changes caused by H diminuta in the small in-testine of rats have been reported (Dwinell et al 1994 19951998) altering intestinal motility such that contractility is in-creased and propulsion is decreased The myoelectric alter-ations could be detected first at 8 days postinfection and dis-appeared within 24 hr after the worms were removed by praz-iquantel The alterations were induced in tapeworm-naive ratsby administration directly into the intestine of worm homog-enates or tegument-enriched fractions Whether the myoelectricalterations have any relationship to the crowding effect is amatter for conjecture at present but their concurrence in timeduring worm development is at least a remarkable coinci-dence It is possible that decreased propulsion slows intestinaltransit increasing the length of time that worms are surroundedby nutrients from the host meal

Host immune response

Our knowledge of the host immune response against adultcestodes especially H diminuta has been reviewed recently(Andreassen et al 1999) and those findings need not be sum-marized in detail here Contrary to opinion prevalent 40 yr agoit is now clear that H diminuta stimulates an immune responseresulting in antibody production and intestinal inflammatory re-

action Immune phenomena can be demonstrated most easilywith H diminuta in mice but effects in rats are more subtlepresumably resulting from the long coevolution of rat and tape-worm Effects appear to vary with rat strain feeding regimeage and with worm strain (Andreassen et al 1999) Interest-ingly no crowding effect was observed either in the tapewormsor the acanthocephalans in hamsters infected concurrently withH diminuta and M moniliformis (Holmes 1962)

Destrobilation and expulsion most commonly when someworms in a crowded infection are expelled are attributed tohost immune response Such phenomena usually have been ob-served in chronic infections ie from a few to many weekspostinfection Hopkins and Andreassen (1991) reported thatwhen H diminuta in a rat were expelled chemotherapeuticallyand the hosts were reinfected at various times thereafter growthof the secondary worms was inhibited The depressive effectwaned rapidly during the first few weeks after the primary in-fection was expelled but it could still be detected as long as17 mo later They argued that if the host immune responseinhibited growth of secondary worms then the primary wormswould have been subjected to the same conditions and that adynamic equilibrium would be reached between the immuneresponse in the gut and the mass of cestode tissue They be-lieved that reaching that equilibrium not a crowding effectlimited the size of the worms to a level compatible with hostsurvival

Conclusion

In their review Andreassen et al (1999) state several timesthat the crowding effect is due to the host inflammatory re-sponse and that lsquolsquoit is clearly not due to competition for car-bohydrate rsquorsquo Yet at another point in the review they saylsquolsquoThe cause of these reactions between adult tapeworms [iethe inverse relationship between number of worms present andworm size] is probably a combination of intraspecific compe-tition for space and food secretion by the worms of so-calledlsquocrowding substancesrsquo and host immune reactionsrsquorsquo Based onobservations summarized in the present paper we can concludethe following (1) Competition among the worms for availablehost dietary carbohydrate at least when the cestodes approachmaximum size is compatible both with our best estimates ofglucose available to the worms in hosts fed normal diets andwith analyses of worms from hosts fed carbohydrate-deficientdiets (2) Some compounds secreted by the worms in vitro in-hibit DNA synthesis and inhibit growth of the worms in vivomimicking a crowding effect (3) Under certain circumstancesinflammatory reactions in the host gut can inhibit growth of thetapeworms One of the foregoing or some combination thereofprobably explains the crowding effect Clarification of the op-erational mechanism at the molecular level would be of greatinterest

LITERATURE CITED

ANDREASSEN J E M BENNET-JENKINS AND C BRYANT 1999 Immu-nology and biochemistry of Hymenolepis diminuta In Advances inparasitology Vol 42 J R Baker R Muller and D Rollinson(eds) Academic Press London p 223ndash275

BOLLA R I AND L S ROBERTS 1971 Developmental physiology ofcestodes X The effect of crowding on carbohydrate levels and on

ROBERTSmdashTHE CROWDING EFFECT REVISITED 211

RNA DNA and protein synthesis in Hymenolepis diminuta Com-parative Biochemistry and Physiology 40A 777ndash787

BUSH A O AND J M LOTZ 1999 The ecology of lsquolsquocrowdingrsquorsquo Jour-nal of Parasitology 86 212ndash213

DAVIS R E 1982 Nucleotide metabolism in the rat tapeworm Hy-menolepis diminuta PhD Thesis University of MassachusettsAmherst Massachusetts 170 p

DENDINGER J E AND L S ROBERTS 1977 Glycogen synthase in therat tapeworm Hymenolepis diminutamdashI Enzyme activity duringdevelopment and with crowding Comparative Biochemistry andPhysiology 58B 215ndash219

DWINELL M B P BASS AND J A OAKS 1994 Intestinal myoelectricalterations in rats chronically infected with the tapeworm Hyme-nolepis diminuta American Journal of Physiology 267 G851ndashG858

AND 1995 Praziquantel treatment normalizesintestinal myoelectric alterations associated with Hymenolepis dim-inuta-infected rats Journal of Parasitology 81 979ndash984

AND 1998 Hymenolepis diminuta fractionsbut not previous tapeworm infection stimulate intestinal myoelec-tric alterations in vivo in the rat Journal of Parasitology 84 673ndash680

HENDERSON D 1977 The effect of worm age weight and number inthe infection on absorption of glucose by Hymenolepis diminutaParasitology 75 277ndash284

HOLMES J C 1961 Effects of concurrent infections on Hymenolepisdiminuta (Cestoda) and Moniliformis dubius (Acanthocephala) IGeneral effects and comparison with crowding Journal of Parasi-tology 47 209ndash216

1962 Effects of concurrent infections on Hymenolepis dimi-nuta and Moniliformis dubius (Acanthocephala) III Effects inhamsters Journal of Parasitology 48 97ndash100

HOPKINS C A AND J ANDREASSEN 1991 Inhibition of growth of atapeworm Hymenolepis diminuta in its normal host (rat) Interna-tional Journal for Parasitology 21 47ndash55

INSLER G D AND L S ROBERTS 1980 Developmental physiology of

cestodes XVI Effects of certain excretory products on incorpora-tion of 3H-thymidine into DNA of Hymenolepis diminuta Journalof Experimental Zoology 211 55ndash61

MEAD R W AND L S ROBERTS 1972 Intestinal digestion and ab-sorption of starch in the intact rat Effects of cestode (Hymenolepisdiminuta) infection Comparative Biochemistry and Physiology41A 749ndash760

PLATZER E G AND L S ROBERTS 1969 Developmental physiologyof cestodes V Effects of vitamin deficient diets and host coproph-agy prevention on development of Hymenolepis diminuta Journalof Parasitology 55 1143ndash1152

AND 1970 Developmental physiology of cestodes VIEffect of host riboflavin deficiency on Hymenolepis diminuta Ex-perimental Parasitology 28 393ndash398

READ C P 1951 The lsquolsquocrowding effectrsquorsquo in tapeworm infections Jour-nal of Parasitology 37 174ndash178

1959 The role of carbohydrates in the biology of cestodesVIII Some conclusions and hypotheses Experimental Parasitology8 365ndash382

ROBERTS L S 1961 The influence of population density on patternsand physiology of growth in Hymenolepis diminuta (Cestoda Cy-clophyllidea) in the definitive host Experimental Parasitology 11332ndash371

1966 Developmental physiology of cestodes I Host dietarycarbohydrate and the lsquolsquocrowding effectrsquorsquo in Hymenolepis diminutaExperimental Parasitology 18 305ndash310

1980 Development of Hymenolepis diminuta in its definitivehost In Biology of the tapeworm Hymenolepis diminuta H P Arai(ed) Academic Press New York p 357ndash423

AND F N MONG 1069 Developmental physiology of cestodesIV In vitro development of Hymenolepis diminuta in presence andabsence of oxygen Experimental Parasitology 26 166ndash174

STARLING J A 1975 Tegumental carbohydrate transport in intestinalhelminths Correlation between mechanisms of membrane transportand the biochemical environment of absorptive surfaces Transac-tions of the American Microscopical Society 94 508ndash523

ROBERTSmdashTHE CROWDING EFFECT REVISITED 211

RNA DNA and protein synthesis in Hymenolepis diminuta Com-parative Biochemistry and Physiology 40A 777ndash787

BUSH A O AND J M LOTZ 1999 The ecology of lsquolsquocrowdingrsquorsquo Jour-nal of Parasitology 86 212ndash213

DAVIS R E 1982 Nucleotide metabolism in the rat tapeworm Hy-menolepis diminuta PhD Thesis University of MassachusettsAmherst Massachusetts 170 p

DENDINGER J E AND L S ROBERTS 1977 Glycogen synthase in therat tapeworm Hymenolepis diminutamdashI Enzyme activity duringdevelopment and with crowding Comparative Biochemistry andPhysiology 58B 215ndash219

DWINELL M B P BASS AND J A OAKS 1994 Intestinal myoelectricalterations in rats chronically infected with the tapeworm Hyme-nolepis diminuta American Journal of Physiology 267 G851ndashG858

AND 1995 Praziquantel treatment normalizesintestinal myoelectric alterations associated with Hymenolepis dim-inuta-infected rats Journal of Parasitology 81 979ndash984

AND 1998 Hymenolepis diminuta fractionsbut not previous tapeworm infection stimulate intestinal myoelec-tric alterations in vivo in the rat Journal of Parasitology 84 673ndash680

HENDERSON D 1977 The effect of worm age weight and number inthe infection on absorption of glucose by Hymenolepis diminutaParasitology 75 277ndash284

HOLMES J C 1961 Effects of concurrent infections on Hymenolepisdiminuta (Cestoda) and Moniliformis dubius (Acanthocephala) IGeneral effects and comparison with crowding Journal of Parasi-tology 47 209ndash216

1962 Effects of concurrent infections on Hymenolepis dimi-nuta and Moniliformis dubius (Acanthocephala) III Effects inhamsters Journal of Parasitology 48 97ndash100

HOPKINS C A AND J ANDREASSEN 1991 Inhibition of growth of atapeworm Hymenolepis diminuta in its normal host (rat) Interna-tional Journal for Parasitology 21 47ndash55

INSLER G D AND L S ROBERTS 1980 Developmental physiology of

cestodes XVI Effects of certain excretory products on incorpora-tion of 3H-thymidine into DNA of Hymenolepis diminuta Journalof Experimental Zoology 211 55ndash61

MEAD R W AND L S ROBERTS 1972 Intestinal digestion and ab-sorption of starch in the intact rat Effects of cestode (Hymenolepisdiminuta) infection Comparative Biochemistry and Physiology41A 749ndash760

PLATZER E G AND L S ROBERTS 1969 Developmental physiologyof cestodes V Effects of vitamin deficient diets and host coproph-agy prevention on development of Hymenolepis diminuta Journalof Parasitology 55 1143ndash1152

AND 1970 Developmental physiology of cestodes VIEffect of host riboflavin deficiency on Hymenolepis diminuta Ex-perimental Parasitology 28 393ndash398

READ C P 1951 The lsquolsquocrowding effectrsquorsquo in tapeworm infections Jour-nal of Parasitology 37 174ndash178

1959 The role of carbohydrates in the biology of cestodesVIII Some conclusions and hypotheses Experimental Parasitology8 365ndash382

ROBERTS L S 1961 The influence of population density on patternsand physiology of growth in Hymenolepis diminuta (Cestoda Cy-clophyllidea) in the definitive host Experimental Parasitology 11332ndash371

1966 Developmental physiology of cestodes I Host dietarycarbohydrate and the lsquolsquocrowding effectrsquorsquo in Hymenolepis diminutaExperimental Parasitology 18 305ndash310

1980 Development of Hymenolepis diminuta in its definitivehost In Biology of the tapeworm Hymenolepis diminuta H P Arai(ed) Academic Press New York p 357ndash423

AND F N MONG 1069 Developmental physiology of cestodesIV In vitro development of Hymenolepis diminuta in presence andabsence of oxygen Experimental Parasitology 26 166ndash174

STARLING J A 1975 Tegumental carbohydrate transport in intestinalhelminths Correlation between mechanisms of membrane transportand the biochemical environment of absorptive surfaces Transac-tions of the American Microscopical Society 94 508ndash523