Physiological consequences of parasite infection in the burrowing mud shrimp, Upogebia pugettensis, a widespread ecosystem engineer
Michele Repetto A and Blaine D. Griffen A B C
+ Author Affiliations
- Author Affiliations
A Marine Science Program, University of South Carolina, Columbia, SC 29208, USA.
B Department of Biological Sciences, University of South Carolina, Columbia, SC 29208, USA.
C Corresponding author. Email: bgriffen@biol.sc.edu
Marine and Freshwater Research 63(1) 60-67 https://doi.org/10.1071/MF11158
Submitted: 6 July 2011 Accepted: 24 September 2011 Published: 8 November 2011
Abstract
The burrowing mud shrimp, Upogebia pugettensis, is an important ecosystem engineer throughout bays and estuaries along the Pacific coast of North America. Populations of U. pugettensis have recently declined throughout its range. A likely reason for this decline is the arrival of an invasive bopyrid isopod parasite, Orthione griffenis, which has colonised the system and increased in prevalence. We tested the following three hypotheses regarding this host–parasite system: (1) parasite infection is correlated with the volume of water processed by the host; (2) infection negatively affects host’s energetic state; and (3) infection causes feminisation in male hosts. We used several physiological and morphological measures to quantify the effects of this parasite infection on U. pugettensis. The parasite appears to have different physiological effects on male and female hosts. Our study provides mixed support for the previous theory that predicted the mechanistic interactions between this host and its new parasite. Recent examples from other systems have demonstrated that invasive parasites can have far-reaching influences when they infect ecosystem engineers. Given the negative effects of O. griffenis on U. pugettensis, this invasive parasite may have similarly large impacts on Pacific North-west estuaries throughout its invaded range.
Additional keywords: host–parasite interactions, Orthione griffenis, Upogebia pugettensis, Yaquina Bay Oregon.
References
Anderson, G. (1975). Metabolic response of caridean shrimp Palaemonetes pugio to infection by adult epibranchial isopod parasite Probopyrus pandalicola. Comparative Biochemistry and Physiology A Physiology 52, 201–207.| Metabolic response of caridean shrimp Palaemonetes pugio to infection by adult epibranchial isopod parasite Probopyrus pandalicola.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2MXlvFSmtbs%3D&md5=c4707c5adb5628e54021e1eb41946c3cCAS |
Anderson, R. M., and May, R. M. (1978). Regulation and stability of host-parasite population interactions. 1. Regulatory processes. Journal of Animal Ecology 47, 219–247.
| Regulation and stability of host-parasite population interactions. 1. Regulatory processes.Crossref | GoogleScholarGoogle Scholar |
Beck, J. T. (1980). Effects of an isopod castrator, Probopyrus pandalicola, on the sex characters of one of its caridean shrimp hosts, Palaemonetes paludosus. The Biological Bulletin 158, 1–15.
| Effects of an isopod castrator, Probopyrus pandalicola, on the sex characters of one of its caridean shrimp hosts, Palaemonetes paludosus.Crossref | GoogleScholarGoogle Scholar |
Bird, E. M. (1982). Population dynamics of thalassinidean shrimps and community effects through sediment modification. Ph.D. Thesis, University of Maryland, College Park, MD.
Brown, G. P., Brooks, R. J., Siddall, M. E., and Desser, S. S. (1994). Parasites and reproductive output in the snapping turtle, Chelydra serpentina. Copeia 1994, 228–231.
| Parasites and reproductive output in the snapping turtle, Chelydra serpentina.Crossref | GoogleScholarGoogle Scholar |
Brown, M. J. F., Loosli, R., and Schmid-Hempel, P. (2000). Condition-dependent expression of virulence in a trypanosome infecting bumblebees. Oikos 91, 421–427.
| Condition-dependent expression of virulence in a trypanosome infecting bumblebees.Crossref | GoogleScholarGoogle Scholar |
Clarke, A. (1984). Lipid composition of two species of Serolis (Crustacea: Isopoda) from Antarctica. British Antarctic Survey Bulletin 64, 37–53.
| 1:CAS:528:DyaL2MXptlaktw%3D%3D&md5=0cf4d021f2e3b31bae921e169e19658cCAS |
Cuzon, G., Gaxiola, G., and Rosas, C. (2008). Nutrition in relation to reproduction in crustaceans. In ‘Reproductive Biology of Crustaceans’. (Ed. E. Mente.) pp. 319–364. (Science Publishers: Enfield, NH.)
D’Andrea, A. F., and DeWitt, T. H. (2009). Geochemical ecosystem engineering by the mud shrimp Upogebia pugettensis (Crustacea: Thalassinidae) in Yaquina Bay, Oregon: density-dependent effects on organic matter remineralization and nutrient cycling. Limnology and Oceanography 54, 1911–1932.
| Geochemical ecosystem engineering by the mud shrimp Upogebia pugettensis (Crustacea: Thalassinidae) in Yaquina Bay, Oregon: density-dependent effects on organic matter remineralization and nutrient cycling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsFKku7rE&md5=c4208ae56ed1f7785fd2c9b93ea90d25CAS |
DeWitt, T. H., D’Andrea, A. F., Brown, C. A., Griffen, B. D., and Eldridge, P. M. (2004). Impact of burrowing shrimp populations on nitrogen cycling and water quality in western North American temperate estuaries. In ‘Proceedings of the Symposium on Ecology of Large Bioturbators in Tidal Flats and Shallow Sediments – from Individual Behavior to their Role as Ecosystem Engineers, 1–2 November 2003’. (Ed. A. Tamaki.) pp. 107–118. (University of Nagasaki: Nagasaki, Japan.)
Dumbauld, B. R., Armstrong, D. A., and Feldman, K. L. (1996). Life-history characteristics of two sympatric thalassinidean shrimps, Neotrypaea californiensis and Upogebia pugettensis, with implications for oyster culture. Journal of Crustacean Biology 16, 689–708.
| Life-history characteristics of two sympatric thalassinidean shrimps, Neotrypaea californiensis and Upogebia pugettensis, with implications for oyster culture.Crossref | GoogleScholarGoogle Scholar |
Dumbauld, B. R., Chapman, J. W., Torchin, M. E., and Kuris, A. M. (2011). Is the collapse of mud shrimp (Upogebia pugettensis) populations along the Pacific coast of North America caused by outbreaks of a previously unknown bopyrid isopod parasite (Orthione griffenis)? Estuaries and Coasts 34, 336–350.
| Is the collapse of mud shrimp (Upogebia pugettensis) populations along the Pacific coast of North America caused by outbreaks of a previously unknown bopyrid isopod parasite (Orthione griffenis)?Crossref | GoogleScholarGoogle Scholar |
Ellison, A. M., Bank, M. S., Clinton, B. D., Colburn, E. A., Elliott, K., Ford, C. R., Foster, D. R., Kloeppel, B. D., Knoepp, J. D., Lovett, G. M., Mohan, J., Orwig, D. A., Rodenhouse, N. L., Sobczak, W. V., Stinson, K. A., Stone, J. K., Swan, C. M., Thompson, J., Von Holle, B., and Webster, J. R. (2005). Loss of foundation species: consequences for the structure and dynamics of forested ecosystems. Frontiers in Ecology and the Environment 3, 479–486.
| Loss of foundation species: consequences for the structure and dynamics of forested ecosystems.Crossref | GoogleScholarGoogle Scholar |
Folch, J., Lees, M., and Stanley, G. H. S. (1957). A simple method for the isolation and purification of total lipids from animal tissues. The Journal of Biological Chemistry 226, 497–509.
| 1:STN:280:DyaG2s%2FnsFCjtw%3D%3D&md5=579b1de1d206fc430da403422c08c8c7CAS |
Gibson, R., and Barker, P. L. (1979). The decapod hepatopancreas. In ‘Oceanography and Marine Biology: an Annual Review, 17’. (Ed. M. Barnes.) pp. 285–346. (Aberdeen University Press: Aberdeen, UK.)
Granath, W. O., and Esch, G. W. (1983). Survivorship and parasite-induced host mortality among mosquitofish in a predator-free, North Carolina cooling reservoir. American Midland Naturalist 110, 314–323.
| Survivorship and parasite-induced host mortality among mosquitofish in a predator-free, North Carolina cooling reservoir.Crossref | GoogleScholarGoogle Scholar |
Griffen, B. D. (2009). Effects of a newly invasive parasite on the burrowing mud shrimp, a widespread ecosystem engineer. Marine Ecology Progress Series 391, 73–83.
| Effects of a newly invasive parasite on the burrowing mud shrimp, a widespread ecosystem engineer.Crossref | GoogleScholarGoogle Scholar |
Griffen, B. D., DeWitt, T. H., and Langdon, C. (2004). Particle removal rates by the mud shrimp Upogebia pugettensis, its burrow, and a commensal clam: effects on estuarine phytoplankton abundance. Marine Ecology Progress Series 269, 223–236.
| Particle removal rates by the mud shrimp Upogebia pugettensis, its burrow, and a commensal clam: effects on estuarine phytoplankton abundance.Crossref | GoogleScholarGoogle Scholar |
Griffen, B. D., Altman, I., Hurley, J., and Mosblack, H. (2011). Reduced fecundity by one invader in the presence of another: a potential mechanism leading to species replacement. Journal of Experimental Marine Biology and Ecology 406, 6–13.
| Reduced fecundity by one invader in the presence of another: a potential mechanism leading to species replacement.Crossref | GoogleScholarGoogle Scholar |
Griffis, R. B., and Suchanek, T. H. (1991). A model of burrow architecture and trophic modes in thalassinidean shrimp (Decapoda: Thalassinidea). Marine Ecology Progress Series 79, 171–183.
| A model of burrow architecture and trophic modes in thalassinidean shrimp (Decapoda: Thalassinidea).Crossref | GoogleScholarGoogle Scholar |
Hara, A., and Radin, N. S. (1978). Lipid extraction of tissues with a low-toxicity solvent. Analytical Biochemistry 90, 420–426.
| Lipid extraction of tissues with a low-toxicity solvent.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1cXmtFWmsL0%3D&md5=833c5279b7aea760e9c30f4570e03652CAS |
Hudson, P. (2005). Parasites, diversity, and the ecosystem. In ‘Parasitism and Ecosystems’. (Eds F. Thomas, F. Renaud and J. F. Guégan.) pp. 1–12. (Oxford University Press: New York.)
Jenkins, J. C., Aber, J. D., and Canham, C. D. (1999). Hemlock woolly adelgid impacts on community structure and N cycling rates in eastern hemlock forests. Canadian Journal of Forest Research-Revue Canadienne De Recherche Forestiere 29, 630–645.
| Hemlock woolly adelgid impacts on community structure and N cycling rates in eastern hemlock forests.Crossref | GoogleScholarGoogle Scholar |
Kennish, R. (1997). Seasonal patterns of food availability: influences on the reproductive output and body condition of the herbivorous crab Grapsus albolineatus. Oecologia 109, 209–218.
| Seasonal patterns of food availability: influences on the reproductive output and body condition of the herbivorous crab Grapsus albolineatus.Crossref | GoogleScholarGoogle Scholar |
Kuris, A. M. (1974). Trophic interactions – similarity of parasitic castrators to parasitoids. The Quarterly Review of Biology 49, 129–148.
| Trophic interactions – similarity of parasitic castrators to parasitoids.Crossref | GoogleScholarGoogle Scholar |
Kuris, A. M., Hechinger, R. F., Shaw, J. C., Whitney, K. L., Aguirre-Macedo, L., Boch, C. A., Dobson, A. P., Dunham, E. J., Fredensborg, B. L., Huspeni, T. C., Lorda, J., Mababa, L., Mancini, F. T., Mora, A. B., Pickering, M., Talhouk, N. L., Torchin, M. E., and Lafferty, K. D. (2008). Ecosystem energetic implications of parasite and free-living biomass in three estuaries. Nature 454, 515–518.
| Ecosystem energetic implications of parasite and free-living biomass in three estuaries.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXovV2mt7k%3D&md5=e4030cfe86a0cee86f9f42a77da5c773CAS |
Kyomo, J. (1988). Analysis of the relationship between gonads and hepatopancreas in males and females of the crab Sesarma intermedia, with reference to resource use and reproduction. Marine Biology 97, 87–93.
| Analysis of the relationship between gonads and hepatopancreas in males and females of the crab Sesarma intermedia, with reference to resource use and reproduction.Crossref | GoogleScholarGoogle Scholar |
Levri, E. P. (1999). Parasite-induced change in host behavior of a freshwater snail: parasitic manipulation or byproduct of infection? Behavioral Ecology 10, 234–241.
| Parasite-induced change in host behavior of a freshwater snail: parasitic manipulation or byproduct of infection?Crossref | GoogleScholarGoogle Scholar |
MacGinitie, G. E. (1930). The natural history of the mud shrimp Upogebia pugettensis (Dana). Annals & Magazine of Natural History 6, 36–44.
| The natural history of the mud shrimp Upogebia pugettensis (Dana).Crossref | GoogleScholarGoogle Scholar |
Mack, R. N. (1985). Invading plants: their potential contribution to population biology. In ‘Studies on Plant Demography: a Festschrift for John L. Harper’. (Ed. J. White.) p. 393. (Academic Press: London.)
Markham, J. C. (1985). A review of the bopyrid isopods infesting caridean shrimps in the northwestern Atlantic Ocean, with special reference to those collected during the Hourglass Cruises in the Gulf of Mexico. Memoirs of the Hourglass Cruises 8, 1–156.
Markham, J. C. (1988). Descriptions and revisions of some species of Isopoda Bopyridae of the north western Atlantic ocean. Zoologische Verhandelingen 246, 1–63.
Markham, J. C. (2004). New species and records of Bopyridae (Crustacea: Isopoda) infesting species of the genus Upogebia (Crustacea: Decapoda: Upogebiidae): the genera Orthione Markham, 1988, and Gyge Cornalia & Panceri, 1861. Proceedings of the Biological Society of Washington 117, 186–198.
May, R. M., and Anderson, R. M. (1978). Regulation and stability of host-parasite population interactions. 2. Destabilizing processes. Journal of Animal Ecology 47, 249–267.
| Regulation and stability of host-parasite population interactions. 2. Destabilizing processes.Crossref | GoogleScholarGoogle Scholar |
Munger, J. C., and Karasov, W. H. (1989). Sublethal parasites and host energy budgets – tapeworm infection in white-footed mice. Ecology 70, 904–921.
| Sublethal parasites and host energy budgets – tapeworm infection in white-footed mice.Crossref | GoogleScholarGoogle Scholar |
Nelson, S. G., Simmons, M.A., and Knight, A.W. (1986). The energy burden of the bopyrid parasite Argeia pauperata (Crustacea, Isopoda) on the grass shrimp Crangon franciscorum (Crustacea, Crangonidae). Comparative Biochemistry and Physiology A Physiology 83, 121–124.
| The energy burden of the bopyrid parasite Argeia pauperata (Crustacea, Isopoda) on the grass shrimp Crangon franciscorum (Crustacea, Crangonidae).Crossref | GoogleScholarGoogle Scholar |
O’Brien, J., and Van Wyk, P. M. (1985). Effects of crustacean parasitic castrators (epicaridean isopods and rizocephalan barnacles) on growth of crustacean hosts. In ‘Crustacean Issues 3: Factors in Adult Growth’. (Ed. A. M. Wenner) pp. 191–218. (A.A. Balkema: Rotterdam.)
Orwig, D. A., Foster, D. R., and Mausel, D. L. (2002). Landscape patterns of hemlock decline in New England due to the introduced hemlock woolly adelgid. Journal of Biogeography 29, 1475–1487.
| Landscape patterns of hemlock decline in New England due to the introduced hemlock woolly adelgid.Crossref | GoogleScholarGoogle Scholar |
Plaistow, S. J., Troussard, J. P., and Cezilly, F. (2001). The effect of the acanthocephalan parasite Pomphorhynchus laevis on the lipid and glycogen content of its intermediate host Gammarus pulex. International Journal for Parasitology 31, 346–351.
| The effect of the acanthocephalan parasite Pomphorhynchus laevis on the lipid and glycogen content of its intermediate host Gammarus pulex.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXisF2gs7g%3D&md5=2c1bd41bfa159d67be820a1ed17ce71bCAS |
Pinho, G. L. L., da Rosa, C. M., Yunes, J. S., Luquet, C. M., Bianchini, A., and Monserrat, J. M. (2003). Toxic effects of microcystins in the hepatopancreas of the estuarine crab Chasmagnathus granulatus (Decapoda, Grapsidae). Comparative Biochemistry and Physiology C – Toxicology & Pharmacology 135, 459–468.
| Toxic effects of microcystins in the hepatopancreas of the estuarine crab Chasmagnathus granulatus (Decapoda, Grapsidae).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3svisVygsg%3D%3D&md5=6040ba634eb74da0e9ff3e26420ed3f0CAS |
Sakai, A. K., Allendorf, F. W., Holt, J. S., Lodge, D. M., Molofsky, J., With, K. A., Baughman, S., Cabin, R. J., Cohen, J. E., Ellstrand, N. C., McCauley, D. E., O’Neil, P., Parker, I. M., Thompson, J. N., and Weller, S. G. (2001). The population biology of invasive species. Annual Review of Ecology and Systematics 32, 305–332.
| The population biology of invasive species.Crossref | GoogleScholarGoogle Scholar |
Sánchez-Paz, A., Garcia-Carreno, F., Hernandez-Lopez, J., Muhlia-Almazan, A., and Yepiz-Plascencia, G. (2007). Effect of short-term starvation on hepatopancreas and plasma energy reserves of the Pacific white shrimp (Litopenaeus vannamei). Journal of Experimental Marine Biology and Ecology 340, 184–193.
| Effect of short-term starvation on hepatopancreas and plasma energy reserves of the Pacific white shrimp (Litopenaeus vannamei).Crossref | GoogleScholarGoogle Scholar |
Schaub, G. A., and Losch, P. (1989). Parasite host interrelationships of the trypanosomatids Trypanosoma cruzi and Blastocrithidia triatomae and the reduviid bug Triatoma infestans – Influence of starvation of the bug. Annals of Tropical Medicine and Parasitology 83, 215–223.
| 1:STN:280:DyaK3c7gtlKmsA%3D%3D&md5=1ffaa9d08d047f3b96ba46f5de35d230CAS |
Smith, A. E., Chapman, J. W., and Dumbauld, B. R. (2008). Population structure and energetics of the bopyrid isopod parasite Orthione griffenis in mud shrimp Upogebia pugettensis. Journal of Crustacean Biology 28, 228–233.
| Population structure and energetics of the bopyrid isopod parasite Orthione griffenis in mud shrimp Upogebia pugettensis.Crossref | GoogleScholarGoogle Scholar |
Stentiford, G. D., Chang, E. S., Chang, S. A., and Neil, D. M. (2001). Carbohydrate dynamics and the crustacean hyperglycemic hormone (CHH): effects of parasitic infection in Norway lobsters (Nephrops norvegicus). General and Comparative Endocrinology 121, 13–22.
| Carbohydrate dynamics and the crustacean hyperglycemic hormone (CHH): effects of parasitic infection in Norway lobsters (Nephrops norvegicus).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXmslarsA%3D%3D&md5=3445c9a4cddbd76593ea4ebaaf4c4316CAS |
Thomas, F., Renaud, F., de Meeus, T., and Poulin, R. (1998). Manipulation of host behaviour by parasites: ecosystem engineering in the intertidal zone? Proceedings of the Royal Society of London. Series B. Biological Sciences 265, 1091–1096.
| Manipulation of host behaviour by parasites: ecosystem engineering in the intertidal zone?Crossref | GoogleScholarGoogle Scholar |
Thomas, F., Poulin, R., de Meeus, T., Guegan, J. F., and Renaud, F. (1999). Parasites and ecosystem engineering: what roles could they play? Oikos 84, 167–171.
| Parasites and ecosystem engineering: what roles could they play?Crossref | GoogleScholarGoogle Scholar |
Thompson, R. K. (1972). Functional morphology of the hind-gut gland of Upogebia pugettensis (Crustacea, Thalassinidea) and its role in burrow construction. Ph.D. Thesis, University of California, Berkeley, CA.
Tingley, M. W., Orwig, D. A., Field, R., and Motzkin, G. (2002). Avian response to removal of a forest dominant: consequences of hemlock woolly adelgid infestations. Journal of Biogeography 29, 1505–1516.
| Avian response to removal of a forest dominant: consequences of hemlock woolly adelgid infestations.Crossref | GoogleScholarGoogle Scholar |
Tompkins, D. M., White, A. R., and Boots, M. (2003). Ecological replacement of native red squirrels by invasive greys driven by disease. Ecology Letters 6, 189–196.
| Ecological replacement of native red squirrels by invasive greys driven by disease.Crossref | GoogleScholarGoogle Scholar |
Tóth, E., and Bauer, R. T. (2007). Gonopore sexing technique allows determination of sex ratios and helper composition in eusocial shrimps. Marine Biology 151, 1875–1886.
| Gonopore sexing technique allows determination of sex ratios and helper composition in eusocial shrimps.Crossref | GoogleScholarGoogle Scholar |
Tucker, B. W. (1930). On the effects of an epicaridean parasite, Gyge branchialis, on Upogebia littoralis. The Quarterly Journal of Microscopical Science 74, 1–11.
Walkey, M., and Meakins, R. H. (1970). An attempt to balance energy budget of a host–parasite system. Journal of Fish Biology 2, 361–372.
| An attempt to balance energy budget of a host–parasite system.Crossref | GoogleScholarGoogle Scholar |
Williams, J. D., and An, J. M. (2009). The cryptogenic parasitic isopod Orthione griffenis Markham, 2004 from the eastern and western Pacific. Integrative and Comparative Biology 49, 114–126.
| The cryptogenic parasitic isopod Orthione griffenis Markham, 2004 from the eastern and western Pacific.Crossref | GoogleScholarGoogle Scholar |
