Hostname: page-component-8448b6f56d-mp689 Total loading time: 0 Render date: 2024-04-25T00:01:33.068Z Has data issue: false hasContentIssue false

Predation on transmission stages reduces parasitism: sea anemones consume transmission stages of a barnacle parasite

Published online by Cambridge University Press:  08 March 2017

CAITLIN R. FONG*
Affiliation:
Department of Biology, California State University Northridge, 18111 Nordhoff Street, Northridge, CA 91330, 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

Summary

While parasites serve as prey, it is unclear how the spatial distribution of parasite predators provides transmission control and influences patterns of parasitism. Because many of its organisms are sessile, the rocky intertidal zone is a valuable but little used system to understand spatial patterns of parasitism and elucidate the underlying mechanisms driving these patterns. Sea anemones and barnacles are important space competitors in the rocky intertidal zone along the Pacific coast of North America. Anemones are voracious, indiscriminate predators; thus, they may intercept infectious stages of parasites before they reach a host. We investigate whether a sea anemone protects an associated barnacle from parasitism by Hemioniscus balani, an isopod parasitic castrator. At Coal Oil Point, Santa Barbara, California USA, 29% of barnacles were within 1 cm from an anemone at the surveyed tidal height. Barnacles associated with anemones had reduced parasite prevalence and higher reproductive productivity than those remote from sea anemones. In the laboratory, anemones readily consumed the transmission stage of the parasite. Hence, anemone consumption of parasite transmission stages may provide a mechanism by which community context regulates parasite prevalence at a local scale. Our results suggest predation may be an important process providing parasite transmission control.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2017 

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

Berger, M. S. (2009). Reproduction of the intertidal barnacle Balanus glandula along an estuarine gradient. Marine Ecology 30, 346353.CrossRefGoogle Scholar
Blower, S. M. and Roughgarden, J. (1987). Population dynamics and parasitic castration: a mathematical model. American Naturalist 129, 730754.Google Scholar
Blower, S. M. and Roughgarden, J. (1988). Parasitic castration: host species preferences, size-selectivity and spatial heterogeneity. Oecologia 75, 512515.CrossRefGoogle ScholarPubMed
Blower, S. M. and Roughgarden, J. (1989 a). Population dynamics and parasitic castration: test of a model. American Naturalist 134, 848858.CrossRefGoogle Scholar
Blower, S. M. and Roughgarden, J. (1989 b). Parasites detect host spatial pattern and density: a field experimental analysis. Oecologia 78, 138141.CrossRefGoogle ScholarPubMed
Brooker, S. (2007). Spatial epidemiology of human schistosomiasis in Africa: risk models, transmission dynamics and control. Transactions of the Royal Society of Tropical Medicine and Hygiene 101, 18.Google Scholar
Brooker, S., Leslie, T., Kolaczinski, K., Mohsen, E., Mehboob, N., Saleheen, S., Khudonazarov, J., Freeman, T., Clements, A., Rowland, M. and Kolaczinski, J. (2006). Spatial epidemiology of Plasmodium vivax, Afghanistan. Emerging Infectious Diseases 12, 16001602.Google Scholar
Byers, J. E., Malek, A. J., Quevillon, L. E., Altman, I., and Keogh, C. L. (2015). Opposing selective pressures decouple pattern and process of parasitic infection over small spatial scale. Oikos 124, 15111519.CrossRefGoogle Scholar
Connell, J. H. (1961). The influence of interspecific competition and other factors on the distribution of the barnacle Chthamalus stellatus . Ecology 42, 710723.CrossRefGoogle Scholar
Cranwell, L. M. and Moore, L. B. (1938). Intertidal Communities of the Poor Knights Islands, New Zealand. Transactions and Proceedings of the Royal Society of New Zealand, New Zealand.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, 11611167.CrossRefGoogle Scholar
Dayton, P. K. (1971). Competition, disturbance, and community organization: the provision and subsequent utilization of space in a rocky intertidal community. Ecological Monographs 41, 351389.Google Scholar
Faust, C., Stallknecht, D., Swayne, D., and Brown, J. (2009). Filter-feeding bivalves can remove avian influenza viruses from water and reduce infectivity. Proceedings of the Royal Society of London B: Biological Sciences 276, 37273735.Google 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, 4649.CrossRefGoogle Scholar
Freuchet, F., Tremblay, R. and Flores, A. A. (2015). Interacting environmental stressors modulate reproductive output and larval performance in a tropical intertidal barnacle. Marine Ecological Progress Series 532, 161175.CrossRefGoogle Scholar
Goudeau, M. (1970). Nouvelle description d'Hemioniscus balani Buchholz, isopode épicaride, au stade de mâle cryptoniscien. Archives de Zoologie Expérimentale et Générale 111, 411448.Google Scholar
Goudeau, M. (1972). Description de l'endosquelette cephalique chez l'Isopode Epicaride Hemioniscus balani Buchholz. Archives de Zoologie Experimentale et Generale 113, 607616.Google Scholar
Hechinger, R. F., Lafferty, K. D., Dobson, A. P., Brown, J. H. and Kuris, A. M. (2011). A common scaling rule for abundance, energetics, and production of parasitic and free-living species. Science 333, 445448.Google Scholar
Hines, A. H. (1978). Reproduction in three species of intertidal barnacles from central California. The Biological Bulletin 154, 262281.Google Scholar
Hopper, J. V., Poulin, R. and Thieltges, D. W. (2008). Buffering role of the intertidal anemone Anthopleura aureoradiata in cercarial transmission from snails to crabs. Journal of Experimental Marine Biology and Ecology 367, 153156.Google Scholar
Johnson, P. T., Dobson, A., Lafferty, K. D., Marcogliese, D. J., Memmott, J., Orlofske, S. A., Poulin, R. and Thieltges, D. W. (2010). When parasites become prey: ecological and epidemiological significance of eating parasites. Trends in Ecology & Evolution 25, 362371.Google Scholar
Kaplan, A. T., Rebhal, S., Lafferty, K. D. and Kuris, A. M. (2009). Small estuarine fishes feed on large trematode cercariae: lab and field investigations. Journal of Parasitology 95, 477480.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, 211232.Google Scholar
Lafferty, K. D. and Kuris, A. M. (2009). Parasitic castration: the evolution and ecology of body snatchers. Trends in Parasitology 25, 564572.Google Scholar
Lafferty, K. D., Dobson, A. P. and Kuris, A. M. (2006). Parasites dominate food web links. Proceedings of the National Academy of Sciences of the United States of America 103, 1121111216.Google Scholar
Leslie, H. M., Breck, E. N., Chan, F., Lubchenco, J. and Menge, B. A. (2005). Barnacle reproductive hotspots linked to nearshore ocean conditions. Proceedings of the National Academy of Sciences of the United States of America 102, 1053410539.Google Scholar
Little, T. J. and Ebert, D. (2000). The cause of parasitic infection in natural populations of Daphnia (Crustacea: Cladocera): the role of host genetics. Proceedings of the Royal Society of London B: Biological Sciences 267, 20372042.Google Scholar
Mkoji, G. M., Hofkin, B. V., Kuris, A. M., Stewart-Oaten, A., Mungai, B. N., Kihara, J. H., Mungai, F., Yundu, J., Mbui, J., Rashid, J. R. and Kariuki, C. H. (1999). Impact of the crayfish Procambarus clarkii on Schistosoma haematobium transmission in Kenya. The American Journal of Tropical Medicine and Hygiene 61, 751759.Google Scholar
Mordecai, E. A., Paaijmans, K. P., Johnson, L. R., Balzer, C., Ben-Horin, T., Moor, E., McNally, A., Pawar, S., Ryan, S. J., Smith, T. C. and Lafferty, K. D. (2013). Optimal temperature for malaria transmission is dramatically lower than previously predicted. Ecology Letters 16, 2230.CrossRefGoogle ScholarPubMed
Mouritsen, K. N. and Poulin, R. (2003). The mud flat anemone-cockle association: mutualism in the intertidal zone? Oecologia 135, 131137.Google Scholar
Orlofske, S. A., Jadin, R. C., Preston, D. L. and Johnson, P. T. (2012). Parasite transmission in complex communities: predators and alternative hosts alter pathogenic infections in amphibians. Ecology 93, 12471253.Google Scholar
Prinz, K., Kelly, T. C., O'Riordan, R. M. and Culloty, S. C. (2009). Non-host organisms affect transmission processes in two common trematode parasites of rocky shores. Marine Biology 156, 23032311.CrossRefGoogle Scholar
Rohr, J. R., Civitello, D. J., Crumrine, P. W., Halstead, N. T., Miller, A. D., Schotthoefer, A. M., Stenoien, C., Johnson, L. B. and Beasley, V. R. (2015). Predator diversity, intraguild predation, and indirect effects drive parasite transmission. Proceedings of the National Academy of Sciences of the United States of America 112, 30083013.Google Scholar
Sokolow, S. H., Huttinger, E., Jouanard, N., Hsieh, M. H., Lafferty, K. D., Kuris, A. M., Riveau, G., Senghor, S., Thiam, C., N'Diaye, A. and Faye, D. S. (2015). Reduced transmission of human schistosomiasis after restoration of a native river prawn that preys on the snail intermediate host. Proceedings of the National Academy of Sciences of the United States of America 112, 96509655.CrossRefGoogle ScholarPubMed
Strauss, A. T., Shocket, M. S., Civitello, D. J., Hite, J. L., Penczykowski, R. M., Duffy, M. A., Cáceres, C. E., and Hall, S. R. (2016). Habitat, predators, and hosts regulate disease in Daphnia through direct and indirect pathways. Ecological Monographs 86, 393411.Google Scholar
Thieltges, D. W., Bordalo, M. D., Caballero Hernández, A., Prinz, K. and Jensen, K. T. (2008). Ambient fauna impairs parasite transmission in a marine parasite-host system. Parasitology 135, 11111116.Google Scholar
Zamer, W. E. (1986). Physiological energetics of the intertidal sea anemone Anthopleura elegantissima . Marine Biology 92, 299314.CrossRefGoogle Scholar