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 inJournal of experimental marine biology and ecology Vol. 524; p. 151284
Main Authors Gooding, Elizabeth L., Kendrick, Michael R., Brunson, Jeff F., Kingsley-Smith, Peter R., Fowler, Amy E., Frischer, Marc E., Byers, James E.
Format Journal Article
LanguageEnglish
Published Elsevier B.V 01.03.2020
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ISSN0022-0981
1879-1697
DOI10.1016/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.
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.
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  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
Language English
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Snippet Parasites can kill hosts directly, but also indirectly, by enhancing susceptibility to environmental factors and biotic interactions. In the United States...
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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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