Hostname: page-component-8448b6f56d-xtgtn Total loading time: 0 Render date: 2024-04-24T23:50:00.744Z Has data issue: false hasContentIssue false
  • English
  • Français

Two's a crowd? Crowding effect in a parasitic castrator drives differences in reproductive resource allocation in single vs double infections

Published online by Cambridge University Press:  08 December 2016

CAITLIN R. FONG Open the ORCID record for CAITLIN R. FONG [Opens in a new window] ,
NANCY A. MORON  and
ARMAND M. KURIS
CAITLIN R. FONG*
Affiliation:
Department of Biology, California State University Northridge, 18111 Nordhoff Street, Northridge, CA 91330, USA
NANCY A. MORON
Affiliation:
Department of Ecology, Evolution, and Marine Biology, University of California, Santa Barbara, CA 93106, USA
ARMAND M. KURIS
Affiliation:
Department of Ecology, Evolution, and Marine Biology, University of California, Santa Barbara, CA 93106, USA
*
*Corresponding author. Department of Biology, California State University Northridge, 18111 Nordhoff Street, Northridge, CA 91330, USA. E-mail: cat.r.fong@gmail.com
Get access Rights & Permissions [Opens in a new window]

Summary

The ‘crowding effect’ is a result of competition by parasites within a host for finite resources. Typically, the severity of this effect increases with increasing numbers of parasites within a host and manifests in reduced body size and thus fitness. Evidence for the crowding effect is mixed – while some have found negative effects, others have found a positive effect of increased parasite load on parasite fitness. Parasites are consumers with diverse trophic strategies reflected in their life history traits. These distinctions are useful to predict the effects of crowding. We studied a parasitic castrator, a parasite that usurps host reproductive energy and renders the host sterile. Parasitic castrators typically occur as single infections within hosts. With multiple parasitic castrators, we expect strong competition and evidence of crowding. We directly assess the effect of crowding on reproductive success in a barnacle population infected by a unique parasitic castrator, Hemioniscus balani, an isopod parasite that infects and blocks reproduction of barnacles. We find (1) strong evidence of crowding in double infections, (2) increased frequency of double infections in larger barnacle hosts with more resources and (3) perfect compensation in egg production, supporting strong space limitation. Our results document that the effects of crowding are particularly severe for this parasitic castrator, and may be applicable to other castrators that are also resource or space limited.

Keywords

parasitic castratorcrowding effectparasite ecologyHemioniscus balaniChthamalus fissusrocky intertidal
Type
Research Article
Information
Parasitology , Volume 144 , Issue 5 , April 2017 , pp. 662 - 668
Check for updates
Copyright
Copyright © Cambridge University Press 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Blower, S. M. and Roughgarden, J. (1987). Population dynamics and parasitic castration: a mathematical model. American Naturalist 129, 730–754.CrossRefGoogle Scholar
Blower, S. M. and Roughgarden, J. (1988). Parasitic castration: host species preferences, size-selectivity and spatial heterogeneity. Oecologia 75, 512–515.Google Scholar
Brown, S. P., De Lorgeril, J., Joly, C. and Thomas, F. (2003). Field evidence for density-dependent effects in the trematode Microphallus papillorobustus in its manipulated host, Gammarus insensibilis . Journal of Parasitology 89, 668–672.CrossRefGoogle ScholarPubMed
Bush, A. O. and Lotz, J. M. (2000). The ecology of “crowding”. Journal of Parasitology 86, 212–213.Google ScholarPubMed
Combes, C. (2001). Parasitism: The Ecology and Evolution of Intimate Interactions. University of Chicago Press.Google Scholar
Crisp, D. J. (1968). Distribution of the parasitic isopod Hemioniscus balani with special reference to the east coast of North America. Journal of the Fisheries Board of Canada 25, 1161–1167.Google Scholar
Desouhant, E., Debouzie, D., Ploye, H. and Menu, F. (2000). Clutch size manipulations in the chestnut weevil, Curculio elephas: fitness of oviposition strategies. Oecologia 122, 493–499.Google Scholar
Fogelman, R. M., Kuris, A. M. and Grutter, A. S. (2009). Parasitic castration of a vertebrate: effect of the cymothoid isopod, Anilocra apogonae, on the five-lined cardinalfish, Cheilodipterus quinquelineatus . International Journal for Parasitology 39, 577–583.CrossRefGoogle ScholarPubMed
Fong, C. R. (2016). High density and strong aggregation do not increase prevalence of the isopod Hemioniscus balani (Buchholz, 1866), a parasite of the acorn barnacle Chthamalus fissus (Darwin, 1854) in California. Journal of Crustacean Biology 36, 46–49.CrossRefGoogle Scholar
Fredensborg, B. L. and Poulin, R. (2005). Larval helminths in intermediate hosts: does competition early in life determine the fitness of adult parasites? International Journal for Parasitology 35, 1061–1070.CrossRefGoogle ScholarPubMed
Götz, P. (1986). Encapsulation in arthropods. In Immunity in Invertebrates (ed. Brehélin, M.) pp. 153–170. Springer, Berlin, Heidelberg.Google Scholar
Hartnoll, R. G. (1967). The effects of sacculinid parasites on two Jamaican crabs. Journal of the Linnean Society of London, Zoology 46(310), 275–295.Google Scholar
Harvey, J. A., Poelman, E. H. and Tanaka, T. (2013). Intrinsic inter- and intraspecific competition in parasitoid wasps. Annual Review of Entomology 58, 333–351.CrossRefGoogle ScholarPubMed
Hechinger, R. F., Lafferty, K. D., Mancini, F. T. III, Warner, R. R. and Kuris, A. M. (2009). How large is the hand in the puppet? Ecological and evolutionary factors affecting body mass of 15 trematode parasitic castrators in their snail host. Evolutionary Ecology 23, 651–667.Google Scholar
Heins, D. C. and Baker, J. A. (2011). Do heavy burdens of Schistocephalus solidus in juvenile threespine stickleback result in disaster for the parasite? Journal of Parasitology 97, 775–778.Google Scholar
Heins, D. C., Baker, J. A. and Martin, H. C. (2002). The “crowding effect” in the cestode Schistocephalus solidus: density-dependent effects on plerocercoid size and infectivity. Journal of Parasitology 88, 302–307.Google Scholar
Hofsvang, T. (1988). Mechanisms of host discrimination and intraspecific competition in the aphid parasitoid Ephedrus cerasicola . Entomologia Experimentalis et Applicata, 48, 233–239.CrossRefGoogle Scholar
Holmes, J. C. (1961). Effects of concurrent infections on Hymenolepis diminuta (Cestoda) and Moniliformis dubius (Acanthocephala). I. General effects and comparison with crowding. Journal of Parasitology 47, 209–216.Google Scholar
Holmes, J. C. (1962 a). Effects of concurrent infections on Hymenolepis diminuta (Cestoda) and Moniliformis dubius (Acanthocephala). II. Effects on growth. Journal of Parasitology 48, 87–96.Google Scholar
Holmes, J. C. (1962 b). Effects of concurrent infections on Hymenolepis diminuta (Cestoda) and Moniliformis dubius (Acanthocephala). III. Effects in hamsters. Journal of Parasitology 48, 97–100.CrossRefGoogle Scholar
Keasar, T., Segoli, M., Barak, R., Steinberg, S., Giron, D., Strand, M. R., Bouskila, A. and Harari, A. R. (2006). Costs and consequences of superparasitism in the polyembryonic parasitoid Copidosoma koehleri (Hymenoptera: Encyrtidae). Ecological Entomology 31, 277–283.Google Scholar
Kuris, A. M. (1974). Trophic interactions: similarity of parasitic castrators to parasitoids. Quarterly Review of Biology 49, 129–148.Google Scholar
Kuris, A. M. (2003). Evolutionary ecology of trophically transmitted parasites. Journal of Parasitology 89 (Suppl.), S96–S100.Google Scholar
Kuris, A. M. (2005). Trophic transmission of parasites and host behaviour modification. Behavioural Processes 68, 215–217.Google Scholar
Kuris, A. M. and Lafferty, K. D. (2000). Parasite-host modeling meets reality: adaptive peaks and their ecological attributes. Evolutionary Biology of Host–Parasite Relationships: Theory Meets Reality (ed. Poulin, R., Morand, S. & Skorping, A.) 9–26.Google Scholar
Kuris, A. M., Poinar, G. O. and Hess, R. T. (1980). Post-larval mortality of the endoparasitic isopod castrator Portunion conformis (Epicaridea: Entoniscidae) in the shore crab, Hemigrapsus oregonensis, with a description of the host response. Parasitology 80, 211–232.CrossRefGoogle Scholar
Lafferty, K. D. and Kuris, A. M. (2002). Trophic strategies, animal diversity and body size. Trends in Ecology & Evolution 17, 507–513.CrossRefGoogle Scholar
Lafferty, K. D. and Kuris, A. M. (2009). Parasitic castration: the evolution and ecology of body snatchers. Trends in Parasitology 25, 564–572.Google Scholar
Lafferty, K. D. and Morris, A. K. (1996). Altered behavior of parasitized killifish increases susceptibility to predation by bird final hosts. Ecology 77, 1390–1397.Google Scholar
Lafferty, K. D., DeLeo, G., Briggs, C. J., Dobson, A. P., Gross, T. and Kuris, A. M. (2015). A general consumer-resource population model. Science 349(6250), 854–857.Google Scholar
Lalonde, R. G. and Roitberg, B. D. (1992). Host selection behavior of a thistle-feeding fly: choices and consequences. Oecologia 90, 534–539.Google Scholar
Lanciani, C.A. (1984). Crowding in the parasitic stage of the water mite Hydrachna virella (Acari: Hydrachnidae). The Journal of Parasitology 70, 270–272.Google Scholar
Lowrie, F. M., Behnke, J. M. and Barnard, C. J. (2004). Density-dependent effects on the survival and growth of the rodent stomach worm Protospirura muricola in laboratory mice. Journal of Helminthology 78, 121–128.Google Scholar
Munoz, G. and George-Nascimento, M. (1999). Reciprocal reproductive effects in the symbiosis between ghost shrimps (Decapoda: Thalassinidea) and bopyrid isopods (Isopoda: Epicaridea) at Lenga, Chile. Revista Chilena de Historia Natural 72, 49–56.Google Scholar
Pollitt, L., Churcher, T. S., Dawes, E. J., Khan, S. M., Sajid, M., Basáñez, M. G., Colegrave, N. and Reece, S. E. (2013). Costs of crowding for the transmission of malaria parasites. Evolutionary Applications 6, 617–629.CrossRefGoogle ScholarPubMed
Poulin, R., Curtis, M. A. and Rau, M. E. (1991). Size, behaviour, and acquisition of ectoparasitic copepods by brook trout, Salvelinus fontinalis . Oikos 61, 169–174.Google Scholar
Poulin, R., Giari, L., Simoni, E. and Dezfuli, B. (2003). Effects of conspecifics and heterospecifics on individual worm mass in four helminth species parasitic in fish. Parasitology Research 90, 143–147.Google Scholar
Read, C. P. (1951). The “crowding effect” in tapeworm infections. Journal of Parasitology 37, 174–178.Google Scholar
Reitz, S. (1995). Superparasitism and intraspecific competition by the solitary larval-pupal parasitoid Archytas marmoratus (Diptera: Tachinidae). Florida Entomologist 78, 578–585.Google Scholar
Roberts, L. S. (2000). The crowding effect revisited. Journal of Parasitology 86, 209–211.Google ScholarPubMed
Roccatagliata, D. and Jordá, M. T. (2002). Infestation of the fiddler crab Uca uruguayensis by Leidya distorta (Isopoda, Bopyridae) from the Rio de la Plata estuary, Argentina. Journal of Crustacean Biology 22, 69–82.Google Scholar
Serafim, L. R., da Silva, J. P. G., de Paiva, N. C. N., dos Santos, H. A., Silva, M. D. G. Q., Carneiro, C. M., Dias, S. R. C. and Rabelo, É. M. L. (2014). The crowding effect in Ancylostoma ceylanicum: density-dependent effects on an experimental model of infection. Parasitology Research 113, 4611–4621.Google Scholar
Shostak, A.W., Walsh, J.G. and Wong, Y. C. (2008). Manipulation of host food availability and use of multiple exposures to assess the crowding effect on Hymenolepis diminuta in Tribolium confusum. Parasitology 135, 1019–1033.CrossRefGoogle ScholarPubMed
Weinersmith, K. L., Warinner, C. B., Tan, V., Harris, D. J., Mora, A. B., Kuris, A. M., Lafferty, K. D. and Hechinger, R. F. (2014). A lack of crowding? Body size does not decrease with density for two behavior-manipulating parasites. Integrative and Comparative Biology 54, 184–192.Google Scholar
Yao, G., Huffman, J.E. and Fried, B. (1991). The effects of crowding on adults of Echinostoma caproni in experimentally infected golden hamsters. Journal of Helminthology 65, 248–254.Google Scholar