Hostname: page-component-848d4c4894-xm8r8 Total loading time: 0 Render date: 2024-06-23T02:46:47.829Z Has data issue: false hasContentIssue false
  • English
  • Français

Environmental factors drive the release of Perkinsus marinus from infected oysters

Published online by Cambridge University Press:  23 December 2020

Sarah A. Gignoux-Wolfsohn Open the ORCID record for Sarah A. Gignoux-Wolfsohn [Opens in a new window] ,
Matilda S. R. Newcomb ,
Gregory M. Ruiz  and
Katrina M. Pagenkopp Lohan
Sarah A. Gignoux-Wolfsohn*
Affiliation:
Marine Disease Ecology Laboratory, Smithsonian Environmental Research Center, Edgewater, MD21037, USA Marine Invasions Research Laboratory, Smithsonian Environmental Research Center, Edgewater, MD21037, USA
Matilda S. R. Newcomb
Affiliation:
Marine Disease Ecology Laboratory, Smithsonian Environmental Research Center, Edgewater, MD21037, USA
Gregory M. Ruiz
Affiliation:
Marine Invasions Research Laboratory, Smithsonian Environmental Research Center, Edgewater, MD21037, USA
Katrina M. Pagenkopp Lohan
Affiliation:
Marine Disease Ecology Laboratory, Smithsonian Environmental Research Center, Edgewater, MD21037, USA
*
Author for correspondence: Sarah A. Gignoux-Wolfsohn, E-mail: gw.sarah@gmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Since the discovery of Perkinsus marinus as the cause of dermo disease in Crassostrea virginica, salinity and temperature have been identified as the main environmental drivers of parasite prevalence. However, little is known about how these variables affect the movement of the parasite from host to water column. In order to elucidate how environmental factors can influence the abundance of this parasite in the water column, we conducted a series of experiments testing the effects of time of day, temperature and salinity on the release of P. marinus cells from infected oysters. We found that P. marinus cells were released on a diurnal cycle, with most cells released during the hottest and brightest period of the day (12:00–18:00). Temperature also had a strong and immediate effect on the number of cells released, but salinity did not, only influencing the intensity of infection over the course of several months. Taken together, our results demonstrate that (1) the number of parasites in the water column fluctuates according to a diurnal cycle, (2) temperature and salinity act on different timescales to influence parasite abundance, and (3) live infected oysters may substantially contribute to the abundance of transmissive parasites in the water column under particular environmental conditions.

Type
Research Article
Information
Parasitology , Volume 148 , Issue 5 , April 2021 , pp. 532 - 538
Check for updates
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

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

Allam, B, Carden, WE, Ward, JE, Ralph, G, Winnicki, S and Pales Espinosa, E (2013) Early host-pathogen interactions in marine bivalves: evidence that the alveolate parasite Perkinsus marinus infects through the oyster mantle during rejection of pseudofeces. Journal of Invertebrate Pathology 113, 26–34.CrossRefGoogle ScholarPubMed
Andrews, JD (1965) Infection experiments in nature with Dermocystidium marinum in Chesapeake Bay. Chesapeake Science 6, 60–67.CrossRefGoogle Scholar
Andrews, JD (1988) Epizootiology of the disease caused by the oyster pathogen Perkinsus marinus and its effects on the oyster industry. American Fisheries Society Special Publication 18, 47–63.Google Scholar
Andrews, JD and Hewatt, WG (1957) Oyster mortality studies in Virginia. II. The fungus disease caused by Dermocystidium marinum in oysters of Chesapeake bay. Ecological Monographs 27, 1–25.CrossRefGoogle Scholar
Andrews, JD, Hoese, HD and Wood, JL (1962) Oyster mortality studies in Virginia 0.3. Epizootiology of a disease caused by Haplosporidium costale Wood and Andrews. Journal of Insect Pathology 4, 327.Google Scholar
Audemard, C, Ragone Calvo, LM, Paynter, KT, Reece, KS and Burreson, EM (2006) Real-time PCR investigation of parasite ecology: in situ determination of oyster parasite Perkinsus marinus transmission dynamics in lower Chesapeake Bay. Parasitology 132, 827–842.CrossRefGoogle ScholarPubMed
Bates, D, Maechler, M, Bolker, B, Walker, S, Christensen, RHB, Singmann, H, Dai, B, Scheipl, F, Grothendieck, G and Green, P (2018) Package ‘lme4’. Version 1, 17.Google Scholar
Ben-Horin, T, Bidegain, G, Huey, L, Narvaez, DA and Bushek, D (2015) Parasite transmission through suspension feeding. Journal of Invertebrate Pathology 131, 155–176.CrossRefGoogle ScholarPubMed
Bidegain, G, Powell, EN, Klinck, JM, Ben-Horin, T and Hofmann, EE (2016) Microparasitic disease dynamics in benthic suspension feeders: infective dose, non-focal hosts, and particle diffusion. Ecological Modelling 328, 44–61.CrossRefGoogle Scholar
Bushek, D, Ford, SE and Chintala, MM (2002) Comparison of in vitro-cultured and wild-type Perkinsus marinus. III. Fecal elimination and its role in transmission. Diseases of Aquatic Organisms 51, 217–225.CrossRefGoogle ScholarPubMed
Calvo, LMR, Dungan, CF, Roberson, BS and Burreson, EM (2003) Systematic evaluation of factors controlling Perkinsus marinus transmission dynamics in lower Chesapeake Bay. Diseases of Aquatic Organisms 56, 75–86.CrossRefGoogle Scholar
Chu, FE and Greene, KH (1989a) Effect of temperature and salinity on in vitro culture of the oyster pathogen, Perkinus marinus (Apicomplexa: Perkinsea). Journal of Invertebrate Pathology 53, 260–268.CrossRefGoogle Scholar
Chu, FLE and Greene, KH (1989b) Effect of temperature and salinity on in vitro culture of the oyster pathogen, Perkinsus-marinus (Apicomplexa – Perkinsea). Journal of Invertebrate Pathology 53, 260–268.CrossRefGoogle Scholar
Chu, FE and La Peyre, JF (1993) Perkinsus marinus susceptibility and defense-related activities in eastern oysters Crassostrea virginica: temperature effects. Diseases of Aquatic Organisms 16, 223–234.CrossRefGoogle Scholar
Chu, FE and Volety, AK (1997) Disease processes of the parasite Perkinsus marinus in eastern oyster Crassostrea virginica: minimum dose for infection initiation, and interaction of temperature, salinity, and infective cell dose. Diseases of Aquatic Organisms 28, 61–68.CrossRefGoogle Scholar
Chu, FE, La Peyre, JF and Burreson, CS (1993) Perkinsus marinus infection and potential defense-related activities in eastern oysters, Cassostrea virginica: salinity effects. Journal of Invertebrate Pathology 62, 226–232.CrossRefGoogle Scholar
Chu, FE, Lund, E, Soudant, P and Harvey, E (2002) De novo arachidonic acid synthesis in Perkinsus marinus, a protozoan parasite of the eastern oyster Crassostrea virginica. Molecular and Biochemical Parasitology 119, 179–190.CrossRefGoogle ScholarPubMed
Comeau, LA, Mayrand, É and Mallet, A (2012) Winter quiescence and spring awakening of the Eastern oyster Crassostrea virginica at its northernmost distribution limit. Marine Biology 159, 2269–2279.CrossRefGoogle Scholar
Cook, T, Folli, M, Klinck, J, Ford, SE and Miller, JR (1998) The relationship between increasing sea-surface temperature and the northward spread of Perkinsus marinus (Dermo) disease epizootics in oysters. Estuarine, Coastal and Shelf Science 46, 587–597.CrossRefGoogle Scholar
da Silva, PM, Vianna, RT, Guertler, C, Ferreira, LP, Santana, LN, Fernandez-Boo, S, Ramilo, A, Cao, A and Villalba, A (2013) First report of the protozoan parasite Perkinsus marinus in South America, infecting mangrove oysters Crassostrea rhizophorae from the Paraiba River (NE, Brazil). Journal of Invertebrate Pathology 113, 96–103.CrossRefGoogle Scholar
Dungan, CF and Bushek, D (2015) Development and applications of Ray's fluid thioglycollate media for detection and manipulation of Perkinsus spp. pathogens of marine molluscs. Journal of Invertebrate Pathology 131, 68–82.CrossRefGoogle Scholar
Ehrich, MK and Harris, LA (2015) A review of existing eastern oyster filtration rate models. Ecological Modelling 297, 201–212.CrossRefGoogle Scholar
Fisher, WS, Gauthier, JD and Winstead, JT (1992) Infection intensity of Perkinsus marinus disease in Crassostrea virginica (Gmelin, 1791) from the Gulf of Mexico maintained under different laboratory conditions. Journal of Shellfish Research 11, 363–369.Google Scholar
Ford, SE (1996) Range extension by the oyster parasite Perkinsus marinus into the northeastern United States: response to climate change? Oceanographic Literature Review 12, 1265.Google Scholar
Ford, SE and Chintala, MM (2006) Northward expansion of a marine parasite: testing the role of temperature adaptation. Journal of Experimental Marine Biology and Ecology 339, 226–235.CrossRefGoogle Scholar
Galtsoff, PS (1928) The effect of temperature on the mechanical activity of the gills of the oyster (Ostrea virginica Gm.). The Journal of General Physiology 11, 415–431.CrossRefGoogle Scholar
Hewatt, WG and Andrews, JD (1954) Oyster mortality studies in Virginia. 1. Mortality of oysters in trays at Gloucester Point, York River. Texas Journal of Science 2, 121.Google Scholar
Hoese, HD (1962) Studies on oyster scavengers and their relations to the fungus Dermocystidium marinum. Proceedings of the National Shellfisheries Association 53, 161.Google Scholar
La Peyre, M, Casas, SM and La Peyre, JF (2006) Salinity effects on viability, metabolic activity and proliferation of three Perkinsus species. Diseases of Aquatic Organisms 71, 59–74.CrossRefGoogle ScholarPubMed
La Peyre, MK, Casas, SM, Villalba, A and La Peyre, JF (2008) Determination of the effects of temperature on viability, metabolic activity and proliferation of two Perkinsus species, and its significance to understanding seasonal cycles of perkinsosis. Parasitology 135, 505–519.CrossRefGoogle ScholarPubMed
Mackin, JG (1951) Histopathology of infection of Crassostrea virginica by Dermocystidium marinum Mackin, Owen, and Collier. Bulletin of Marine Science of the Gulf and Caribbean 1, 72–87.Google Scholar
Malek, JC and Breitburg, DL (2016) Effects of air-exposure gradients on spatial infection patterns of Perkinsus marinus in the eastern oyster Crassostrea virginica. Diseases of Aquatic Organisms 118, 139–151.CrossRefGoogle ScholarPubMed
Malek, JC and Byers, JE (2017) The effects of tidal elevation on parasite heterogeneity and co-infection in the eastern oyster, Crassostrea virginica. Journal of Experimental Marine Biology and Ecology 494, 32–37.CrossRefGoogle Scholar
Malek, JC and Byers, JE (2018) Responses of an oyster host (Crassostrea virginica) and its protozoan parasite (Perkinsus marinus) to increasing air temperature. PeerJ 6, e5046.CrossRefGoogle Scholar
Maryland Department of Natural Resources. Eyes on the Bay. www.eyesonthebay.netGoogle Scholar
Mat, AM, Massabuau, JC, Ciret, P and Tran, D (2012) Evidence for a plastic dual circadian rhythm in the oyster Crassostrea gigas. Chronobiology International 29, 857–867.CrossRefGoogle ScholarPubMed
Pagenkopp Lohan, KM, Hill-Spanik, KM, Torchin, ME, Aquirre-Macedo, M, Fleischer, RC and Ruiz, GM (2016) Richness and distribution of tropical oyster parasites in two oceans. Parasitology 143, 1119–1132.CrossRefGoogle ScholarPubMed
Paynter, KT and Burreson, EM (1991) Effects of Perkinsus marinus infection in the eastern oyster, Crassostrea virginica: II. Disease development and impact on growth rate at different salinities. Journal of Shellfish Research 10, 425–431.Google Scholar
Ragone Calvo, LM and Burreson, EM (1993) Effect of salinity on infection progression and pathogenicity of Perkinsus marinus in the eastern oyster, Crassostrea virginica (gmelin). Journal of Shellfish Research 12, 1–7.Google Scholar
Ray, SM (1954) Biological studies of Dermocystidium marinum a Fungus Parasite of Oysters. Biology, Doctor of Philosophy dissertation. Houston, Texas: The Rice Institute.Google Scholar
Reece, KS, Dungan, CF and Burreson, EM (2008) Molecular epizootiology of Perkinsus marinus and P. chesapeaki infections among wild oysters and clams in Chesapeake Bay, USA. Diseases of Aquatic Organisms 82, 237–248.CrossRefGoogle ScholarPubMed
Ripley, B, Venables, B, Bates, DM, Hornik, K, Gebhardt, A, Firth, D and Ripley, MB (2013) Package ‘mass’. Cran R 538.Google Scholar
Schindelin, J, Arganda-Carreras, I, Frise, E, Kaynig, V, Longair, M, Pietzsch, T, Preibisch, S, Rueden, C, Saalfeld, S and Schmid, B (2012) Fiji: an open-source platform for biological-image analysis. Nature Methods 9, 676–682.CrossRefGoogle ScholarPubMed
Soniat, TM, Klinck, JM, Powell, EN and Hofmann, EE (2005) Understanding the success and failure of oyster populations: climatic cycles and Perkinsus marinus. Journal of Shellfish Research 24, 83–93.Google Scholar
Sunila, I and LaBanca, J (2003) Apoptosis in the pathogenesis of infectious diseases of the eastern oyster Crassostrea virginica. Diseases of Aquatic Organisms 56, 163–170.CrossRefGoogle ScholarPubMed
Tarnowski, M (2018) Maryland Oyster Population Status Report. Maryland Department of Natural Resources Shellfish Division of Cooperative Oxford Laboratory.Google Scholar
Tran, D, Nadau, A, Durrieu, G, Ciret, P, Parisot, JP and Massabuau, JC (2011) Field chronobiology of a molluscan bivalve: how the moon and sun cycles interact to drive oyster activity rhythms. Chronobiology International 28, 307–317.CrossRefGoogle Scholar
Villalba, A, Reece, KS, Camino Ordás, M, Casas, SM and Figueras, A (2004) Perkinsosis in molluscs: a review. Aquatic Living Resources 17, 411–432.CrossRefGoogle Scholar
White, ME, Powell, EN, Ray, SM and Wilson, EA (1987) Host-to host transmission of Perkinsus marinus in oyster (Crassostrea virginica) populations by the ectoparasitic snail Boonea impressa (Pyramidellidae). Journal of Shellfish Research 6, 1–5.Google Scholar
Wickham, H (2009) ggplot2: Elegant Graphics for Data Analysis. New York: Springer Science & Business Media.CrossRefGoogle Scholar
Supplementary material: File

Gignoux-Wolfsohn et al. supplementary material

Gignoux-Wolfsohn et al. supplementary material

Download Gignoux-Wolfsohn et al. supplementary material(File)
File 165.5 KB