Black gill increases the susceptibility of white shrimp, Penaeus setiferus (Linnaeus, 1767), to common estuarine predators
Parasites can kill hosts directly, but also indirectly, by enhancing susceptibility to environmental factors and biotic interactions. In the United States South Atlantic Bight region of the northwest Atlantic Ocean, white shrimp (Penaeus setiferus) support a substantial commercial fishery and are al...
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Published in | Journal of experimental marine biology and ecology Vol. 524; p. 151284 |
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Main Authors | , , , , , , |
Format | Journal Article |
Language | English |
Published |
Elsevier B.V
01.03.2020
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Online Access | Get full text |
ISSN | 0022-0981 1879-1697 |
DOI | 10.1016/j.jembe.2019.151284 |
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Abstract | Parasites can kill hosts directly, but also indirectly, by enhancing susceptibility to environmental factors and biotic interactions. In the United States South Atlantic Bight region of the northwest Atlantic Ocean, white shrimp (Penaeus setiferus) support a substantial commercial fishery and are also valuable prey for many marine and estuarine species. Since the late 1990s, a condition known as black gill has been observed in penaeid shrimp in the South Atlantic Bight. In this region, black gill has been linked to an apostome ciliate that elicits an innate immune response in shrimp, manifested through the melanization of gill tissues, which impedes respiratory functions and hemolymph ion regulation. The objective of this study was to determine if black gill subjects shrimp to higher rates of predation by red drum (Sciaenops ocellatus), spotted seatrout (Cynoscion nebulosus), and blue crab (Callinectes sapidus). A series of simultaneous prey choice mesocosm experiments was conducted, during which single-species predators were able to consume shrimp that were both symptomatic and asymptomatic of black gill over a four-hour period. Predator species were 1.4 to 3.0 times more likely to consume symptomatic shrimp than asymptomatic shrimp. The hinderance of shrimp physiology and escape responses due to gill melanization likely increases the vulnerability of shrimp to predation. This study emphasizes that mortality from parasitic infections is not always direct and that black gill may have a significant impact on penaeid shrimp through secondary, or indirect, mortality.
•We examined the effects of black gill on shrimp susceptibility to predation by red drum, spotted seatrout, and blue crabs.•Shrimp symptomatic of black gill were more likely to be consumed than asymptomatic shrimp across all predator species.•Blue crabs fed at the lowest rate but exhibited the strongest preference for symptomatic compared to asymptomatic shrimp. |
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AbstractList | Parasites can kill hosts directly, but also indirectly, by enhancing susceptibility to environmental factors and biotic interactions. In the United States South Atlantic Bight region of the northwest Atlantic Ocean, white shrimp (Penaeus setiferus) support a substantial commercial fishery and are also valuable prey for many marine and estuarine species. Since the late 1990s, a condition known as black gill has been observed in penaeid shrimp in the South Atlantic Bight. In this region, black gill has been linked to an apostome ciliate that elicits an innate immune response in shrimp, manifested through the melanization of gill tissues, which impedes respiratory functions and hemolymph ion regulation. The objective of this study was to determine if black gill subjects shrimp to higher rates of predation by red drum (Sciaenops ocellatus), spotted seatrout (Cynoscion nebulosus), and blue crab (Callinectes sapidus). A series of simultaneous prey choice mesocosm experiments was conducted, during which single-species predators were able to consume shrimp that were both symptomatic and asymptomatic of black gill over a four-hour period. Predator species were 1.4 to 3.0 times more likely to consume symptomatic shrimp than asymptomatic shrimp. The hinderance of shrimp physiology and escape responses due to gill melanization likely increases the vulnerability of shrimp to predation. This study emphasizes that mortality from parasitic infections is not always direct and that black gill may have a significant impact on penaeid shrimp through secondary, or indirect, mortality. Parasites can kill hosts directly, but also indirectly, by enhancing susceptibility to environmental factors and biotic interactions. In the United States South Atlantic Bight region of the northwest Atlantic Ocean, white shrimp (Penaeus setiferus) support a substantial commercial fishery and are also valuable prey for many marine and estuarine species. Since the late 1990s, a condition known as black gill has been observed in penaeid shrimp in the South Atlantic Bight. In this region, black gill has been linked to an apostome ciliate that elicits an innate immune response in shrimp, manifested through the melanization of gill tissues, which impedes respiratory functions and hemolymph ion regulation. The objective of this study was to determine if black gill subjects shrimp to higher rates of predation by red drum (Sciaenops ocellatus), spotted seatrout (Cynoscion nebulosus), and blue crab (Callinectes sapidus). A series of simultaneous prey choice mesocosm experiments was conducted, during which single-species predators were able to consume shrimp that were both symptomatic and asymptomatic of black gill over a four-hour period. Predator species were 1.4 to 3.0 times more likely to consume symptomatic shrimp than asymptomatic shrimp. The hinderance of shrimp physiology and escape responses due to gill melanization likely increases the vulnerability of shrimp to predation. This study emphasizes that mortality from parasitic infections is not always direct and that black gill may have a significant impact on penaeid shrimp through secondary, or indirect, mortality. •We examined the effects of black gill on shrimp susceptibility to predation by red drum, spotted seatrout, and blue crabs.•Shrimp symptomatic of black gill were more likely to be consumed than asymptomatic shrimp across all predator species.•Blue crabs fed at the lowest rate but exhibited the strongest preference for symptomatic compared to asymptomatic shrimp. |
ArticleNumber | 151284 |
Author | Kingsley-Smith, Peter R. Gooding, Elizabeth L. Frischer, Marc E. Kendrick, Michael R. Brunson, Jeff F. Byers, James E. Fowler, Amy E. |
Author_xml | – sequence: 1 givenname: Elizabeth L. surname: Gooding fullname: Gooding, Elizabeth L. email: goodinge@dnr.sc.gov organization: Marine Resources Research Institute, South Carolina Department of Natural Resources, 217 Fort Johnson Road, Charleston, SC 29422, United States of America – sequence: 2 givenname: Michael R. surname: Kendrick fullname: Kendrick, Michael R. email: kendrickm@dnr.sc.gov organization: Marine Resources Research Institute, South Carolina Department of Natural Resources, 217 Fort Johnson Road, Charleston, SC 29422, United States of America – sequence: 3 givenname: Jeff F. surname: Brunson fullname: Brunson, Jeff F. email: brunsonj@dnr.sc.gov organization: Marine Resources Research Institute, South Carolina Department of Natural Resources, 217 Fort Johnson Road, Charleston, SC 29422, United States of America – sequence: 4 givenname: Peter R. surname: Kingsley-Smith fullname: Kingsley-Smith, Peter R. email: kingsleysmithp@dnr.sc.gov organization: Marine Resources Research Institute, South Carolina Department of Natural Resources, 217 Fort Johnson Road, Charleston, SC 29422, United States of America – sequence: 5 givenname: Amy E. surname: Fowler fullname: Fowler, Amy E. email: afowler6@gmu.edu organization: Marine Resources Research Institute, South Carolina Department of Natural Resources, 217 Fort Johnson Road, Charleston, SC 29422, United States of America – sequence: 6 givenname: Marc E. surname: Frischer fullname: Frischer, Marc E. email: marc.frischer@skio.uga.edu organization: University of Georgia, Skidaway Institute of Oceanography, 10 Ocean Science Circle, Savannah, GA 31411, United States of America – sequence: 7 givenname: James E. surname: Byers fullname: Byers, James E. email: jebyers@uga.edu organization: Odum School of Ecology, University of Georgia, 140 East Green Street, Athens, GA 30602, United States of America |
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Keywords | Parasite-host dynamic Parasitism Penaeus (Litopenaeus) setiferus Secondary mortality Predator-prey interaction Shrimp black gill |
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SubjectTerms | Callinectes sapidus crabs Cynoscion nebulosus estuaries fisheries hemolymph innate immunity Litopenaeus setiferus melanization mortality Northwest Atlantic Parasite-host dynamic Parasitism Penaeus (Litopenaeus) setiferus predation Predator-prey interaction Sciaenops ocellatus Secondary mortality shrimp Shrimp black gill |
Title | Black gill increases the susceptibility of white shrimp, Penaeus setiferus (Linnaeus, 1767), to common estuarine predators |
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