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Parasite alteration of host shape: a quantitative approach to gigantism helps elucidate evolutionary advantages

Published online by Cambridge University Press:  19 January 2004

H. O. McCARTHY ,
S. M. FITZPATRICK  and
S. W. B. IRWIN
H. O. McCARTHY
Affiliation:
School of Biological and Environmental Sciences, University of Ulster, Newtownabbey, Belfast, Co. Antrim, N. Ireland BT37 0QB
S. M. FITZPATRICK
Affiliation:
School of Biological and Environmental Sciences, University of Ulster, Newtownabbey, Belfast, Co. Antrim, N. Ireland BT37 0QB
S. W. B. IRWIN
Affiliation:
School of Biological and Environmental Sciences, University of Ulster, Newtownabbey, Belfast, Co. Antrim, N. Ireland BT37 0QB
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Abstract

This investigation quantifies some aspects of the parasite–host relationship between the digenean Microphallus piriformes and its intermediate host Littorina saxatilis, the rough periwinkle. M. piriformes has an abridged life-cycle with no free-living stages, metacercariae remain within host viscera. Noticeable differences in shell shape of parasitized and uninfected periwinkles were investigated. These differences in shell shape were defined by growth parameters of height, diameter and β angle. The relationship between these parameters was examined together with their impact on parasite reproduction. All 3 shape parameters were altered in periwinkles infected by M. piriformes. The alteration in β angle and height increased the available volume for parasites in the shell spire by about 12%. As metacercarial production per sporocyst has been shown to depend on host size, the increased volume enables considerable additional life-time reproduction by the parasite, of approximately 550–850 additional metacercariae in hosts of the usual size range. The form of gigantism found in this study is discussed in relation to previous concepts. It is suggested that gigantism in permanently castrated hosts is adaptive parasite manipulation of host physiology, favoured in parasites with abbreviated life-cycles, when host viability increases parasite transmission, and when an initially small host individual is infected.

Keywords

parasite–host relationshipgigantismLittorina saxatilisMicrophallustrematode
Type
Research Article
Information
Parasitology , Volume 128 , Issue 1 , January 2004 , pp. 7 - 14
Copyright
2004 Cambridge University Press

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References

REFERENCES

BAUDOIN, M. (1975). Host castration as a parasitic strategy. Evolution 29, 335–352.CrossRefGoogle Scholar
CREWS, A. E. & YOSHING, T. P. (1989). Schistosoma mansoni – effect of infection on reproduction and gonadal growth in Biomphalaria glabrata. Experimental Parasitology 68, 302–334.CrossRefGoogle Scholar
D'ARCY THOMPSON, W. (1961). On Growth and Form. Cambridge University Press, Cambridge.
FERNANDEZ, J. & ESCH, G. W. (1991). Effect of parasitism on the growth rate of the pulmonate snail Helisoma anceps. Journal of Parasitology 77, 937–944.CrossRefGoogle Scholar
GORBUSHIN, A. M. (1997). Field evidence of trematode induced gigantism in Hydrobia spp. (Gastropoda: Prosobranchia). Journal of the Marine Biological Association of the United Kingdom 77, 785–800.Google Scholar
GORBUSHIN, A. M. & LEVAKIN, I. A. (1999). The effect of trematode parthenitae on the growth of Onoba aculeus, Littorina saxatilis and L. obtusata (Gastropoda: Prosobranchia). Journal of the Marine Biological Association of the United Kingdom 79, 273–279.Google Scholar
HUGHES, R. N. & ANSWER, P. (1982). Growth, spawning and trematode infection of Littorina littorea (L.) from an exposed shore in North Wales. Journal of Molluscan Studies 48, 321–330.Google Scholar
McCARTHY, H. O. (2000). Adaptive variation in trematode parasite life cycles; implications of 2-host and 3-host cycles for parasite reproductive strategies and transmission. Ph.D. thesis, University of Ulster, Northern Ireland, UK.
McCARTHY, H. O., FITZPATRICK, S. M. & IRWIN, S. W. B. (2000). A transmissible trematode affects the direction and rhythm of movement in a marine gastropod. Animal Behaviour 59, 1161–1166.CrossRefGoogle Scholar
McCARTHY, H. O., FITZPATRICK, S. M. & IRWIN, S. W. B. (2002). Life history and life cycles: Production and behaviour of trematode cercariae in relation to host exploitation and next-host characteristics. Journal of Parasitology 88, 910–918.CrossRefGoogle Scholar
McCLELLAND, G. & BOURNS, T. K. R. (1969). Effects of Trichobilharzia ocellata on growth, reproduction and survival of Lymnaea stagnalis. Experimental Parasitology 24, 137–146.CrossRefGoogle Scholar
MINCHELLA, D. J. (1985). Host life-history variation in response to parasitism. Parasitology 90, 205–216.CrossRefGoogle Scholar
MOURITSEN, K. N., GORBUSHIN, A. & JENSEN, K. T. (1999). Influence of trematode infections on in situ growth rates of Littorina littorea. Journal of the Marine Biological Association of the United Kingdom 79, 425–430.CrossRefGoogle Scholar
MOURITSEN, K. N. & JENSEN, K. T. (1994). The enigma of gigantism – effect of larval trematodes on growth, fecundity, egestion and locomotion in Hydrobia ulvae (Pennant) (Gastropoda: Prosobranchia). Journal of Experimental Marine Biology and Ecology 181, 53–66.CrossRefGoogle Scholar
POPIEL, I. & JAMES, B. L. (1978). The ultrastructure of the tegument of the daughter sporocyst of Microphallus similis (Jäg., 1900) (Digenea: Microphallidae). Parasitology 76, 359–367.Google Scholar
PROBST, S. & KUBE, J. (1999). Histopathological effects of larval trematode infections in mudsnails and their impact on host growth: what causes gigantism in Hydrobia ventrosa (Gastropoda: Prosobranchia)? Journal of Experimental Marine Biology and Ecology 238, 49–68.Google Scholar
ROTHSCHILD, A. & ROTHSCHILD, M. (1939). Some observations on the growth of Peringia ulvae (Pennant) (1777) in the laboratory. Novitates Zoologicae 41, 240–247.Google Scholar
SAS INSTITUTE (1995). Cary N.C.USA.
SAVILLE, D. H., GALAKTIONOV, K. V., IRWIN, S. W. B. & MALKOVA, I. I. (1997). Morphological comparison and identification of metacercariae in the ‘pygmaeus’ group of microphallids, parasites of seabirds in western palaearctic regions. Journal of Helminthology 71, 167–174.CrossRefGoogle Scholar
SOUSA, W. P. (1983). Host life history and the effect of parasitic castration on growth: A field study of Cerithidea californica Haldeman (Gastropoda: Prosobranchia) and its trematode parasites. Journal of Experimental Marine Biology and Ecology 73, 273–296.CrossRefGoogle Scholar
STURROCK, B. M. & STURROCK, R. F. (1970). Laboratory studies of the host–parasite relationship of Schistosoma mansoni and Biomphalaria glabrata from St. Lucia, West Indies. Annals of Tropical Medicine and Parasitology 64, 357–363.CrossRefGoogle Scholar
THÉRON, A. (1985). Le polymorphisme du rythme d'émission des cercaires de Schistosoma mansoni et ses relations avec l'écologie de la transmission du parasite. Vie et Milieu 35, 23–31.Google Scholar