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A Georgia white shrimp displays symptoms of the Black Gill condition around its gills. Courtesy of Rachael Randall and Chelsea Parrish, 2015
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In the Southeast United States, an unidentified parasite is infecting shrimp and presenting new challenges for an already struggling industry. Emerging research in Georgia is investigating the resulting condition, known as Black Gill, to better understand this newest threat to the state’s most valuable commercial fishery. Researchers, shrimpers, ex...
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Citations
... Conversely, an intolerance for risk leads to a willingness to reject an expected benefit in an attempt to avoid possible outcomes that have low probability and high cost. Decision makers are likely to be particularly concerned with risks of infectious diseases that threaten human livelihoods by causing collapses in fisheries and aquaculture stocks upon which stakeholders depend (Mardones et al. 2011;Gambill et al. 2015). ...
Fisheries and aquaculture provide food and economic security, especially in the developing world, but both face challenges from infectious disease. Here, we consider management of disease issues from a structured decision‐making perspective to examine how infectious disease can threaten seafood production and influence management decisions. For both wild fisheries and aquaculture, disease‐management objectives generally aim to mitigate the severity and economic burden of outbreaks. General management strategies include manipulating host densities, reducing system connectivity, conserving or improving habitat, and implementing direct treatments or some other biological interventions. To inform decisions, mathematical models can be used to explore disease dynamics and to forecast the potential effectiveness of alternative management actions. Developing and implementing disease‐management strategies also involve considering uncertainties and balancing competing stakeholder interests and risk tolerances. We conclude by outlining several steps for applying structured decision making that are broadly useful to decision makers facing issues related to disease.
... IntroductIon Shrimp Black Gill (Hyalophysa lynni) is a parasitic ciliate that has been impacting penaeid shrimp populations from the Chesapeake Bay through the Gulf of Mexico (GOM). Hyalophysa lynni has been detected in wild White Shrimp (Litopenaeus setiferus) and Brown Shrimp (Farfantepenaeus aztecus) in the Southeast Atlantic Bight since 1996 (Geer 2003, Gambill et al. 2015, Frischer et al. 2017 and has been confirmed to be present and prolific in both species of penaeid shrimp along the Texas Gulf Coast since at least 2019 (Swinford and Anderson 2021). The symptoms often described as Shrimp Black Gill have only recently been identified as being caused by the parasitic ciliate H. lynni (Landers et al. 2020). ...
Shrimp Black Gill, caused by the apostome ciliate Hyalophysa lynni, is an emerging disease impacting penaeid shrimp populations along the southeast Atlantic Coast and the Gulf of Mexico (GOM). Changing annual environmental conditions may drive infection levels of this parasitic ciliate in these populations, which comprise one of the largest fisheries in the United States. Hyalophysa lynni is established on the Texas Gulf Coast, and prevalence of this parasite has a strong seasonal and spatial trend, likely linked with high temperature and a wide range of estuarine salinities. Texas Parks and Wildlife Department monitored shrimp black gill in 2 penaeid shrimp species, Litopenaeus setiferus and Farfantepenaeus aztecus in 2019, with the aim of observing trends in prevalence along spatial and temporal scales. Hyalophysa lynni was found in all 7 bay systems throughout the study period, and this study is a continuation of that monitoring effort, adding 2 years of data collection (2020 and 2021) to prior research. Throughout the entire sampling period (2019–2021) and coastwide, H. lynni was found in 66% of all shrimp samples collected, although prevalence varied annually. Boosted regression tree modeling indicated that low salinity, high temperature, and time of year (late spring through fall) had a significant relationship with H. lynni prevalence in shrimp along the Texas Gulf Coast. Shrimp Black Gill is likely to continue to be present in GOM shrimp populations, and annual precipitation events and increased water temperatures may amplify the population morbidity within any given year.
... Over the past few decades, a condition known as black gill has been observed at high prevalence levels in white shrimp because of a series of pathogen infection or water quality variables (Dewangan et al., 2015;Fowler et al., 2016;Gambill et al., 2015;Lin et al., 2020). However, there were no reports of BSD on the abdomen of P. vannamei. ...
In Nov 2020, mass mortality of cultured Pacific white shrimp (Litopenaeus vannamei) occurred due to black spot disease (BSD) in some shrimp farms in China. To investigate the disease cause, a potential pathogenic fungus was isolated from melanized lesions of L. vannamei suffering from the BSD syndrome. The fungal isolate was then identified as Fusarium solani based on TEF1α and ITS-gene sequences. The isolate of fungus was used in infection studies. This study used Koch postulates confirmed that the studied agent was causing BSD symptoms in the white leg shrimp, which were significantly symptoms relieved after molting. Results showed that an identical fungus was re-isolated from black lesions after the artificial infection period. Virulence test revealed that F. solani could cause 88.66% mortality within 30 dpi at a dose of 1.015 × 10⁶ CFU/mL, and the LC50 of F. solani at 30 dpi is 3.37 × 10⁴ CFU/mL. The accumulative mortalities also displayed concentration dependence. The histopathological characterization displayed that responses of L. vannamei against F. solani are haemocytic infiltration, encapsulation, melanization, etc. in the black spot lesions. Furthermore, severe infection of F. solani in L. vannamei causes molting failure, and further contributes to the mortality of the diseased individuals. The findings of our study would be useful to provide a theoretical basis for early prevention and control of BSD.
... Shrimp black gill has been observed in wild white shrimp Litopenaeus setiferus and brown shrimp Farfantepenaeus aztecus in the southeast Atlantic penaeid shrimp fishery since 1996 (Gambill et al. 2015;Frischer et al. 2017; P. Geer, Virginia Institute of Marine Science, unpublished data), and unidentified apostome ciliate cysts similar to those associated with sBG were observed in Gulf of Mexico shrimp during the 1970s (Couch 1978;Overstreet 1978). Prevalence of the disease has been increasing in the southeast Atlantic population steadily every year, potentially correlating with a decline in landings in the southeast Atlantic fishery (Frischer et al. 2017). ...
... The previously established range of H. lynni extends from the north-central Gulf of Mexico to the Chesapeake Bay (Gambill et al. 2015;Frischer et al. 2017;Fowler et al. 2018;Landers et al. 2020;Tuckey et al. 2021). Shrimp black gill was first observed in Georgia, which, along with South Carolina, is the center of abundance for recorded sBG prevalence along the U.S. East Coast (Gambill et al. 2015;Frischer et al. 2017;Fowler et al. 2018). ...
... The previously established range of H. lynni extends from the north-central Gulf of Mexico to the Chesapeake Bay (Gambill et al. 2015;Frischer et al. 2017;Fowler et al. 2018;Landers et al. 2020;Tuckey et al. 2021). Shrimp black gill was first observed in Georgia, which, along with South Carolina, is the center of abundance for recorded sBG prevalence along the U.S. East Coast (Gambill et al. 2015;Frischer et al. 2017;Fowler et al. 2018). Recently, penaeid shrimp from the Gulf of Mexico, specifically from Mississippi and Louisiana, have been confirmed to have the same apostome ciliate (H. ...
Shrimp black gill is an emerging disease caused by a parasitic ciliate, Hyalophysa lynni, that attacks gill tissue in white shrimp Litopenaeus setiferus and brown shrimp Farfantepenaeus aztecus and induces an immune response that produces melanized tissue in shrimp gills. This immune response causes necrosis and damage in shrimp gill tissue, which limits shrimp metabolic capability and can lead to high predation mortality among infected individuals. Shrimp black gill was first observed in the southeast Atlantic shrimp fishery in the United States, and this ciliate has been increasing in prevalence in shrimp populations of this region since 2000. The Gulf of Mexico, with its lucrative shrimp fishery and extended warmwater conditions during the year, is a potential region for H. lynni spread. White and brown shrimp were sampled from seven major bays along the Gulf coast of Texas from March to November 2019 and underwent PCR analysis to detect H. lynni presence in gill tissue. From March to November, 65% of the collected shrimp samples tested positive for H. lynni. Samples from all seven bays tested positive for H. lynni, with the upper-coast bays having a significantly higher disease prevalence than lower-coast bays. Both white and brown shrimp samples tested positive for H. lynni; however, white shrimp samples had a significantly higher disease prevalence. Overall, disease prevalence showed a temporal pattern of low prevalence in the spring, peaking during the late fall. Generalized additive mixed models detected a high water temperature and a salinity level of 30‰ or less as significant contributors to high disease prevalence. This study validates the commonality of H. lynni presence in the western Gulf of Mexico, serves as a baseline for future shrimp black gill sampling efforts in this region, and contributes to the understanding and management of potential disease threats to the Texas shrimp fishery.
... In addition to supporting an extensive commercial fishery in the southeastern U.S. (Gillet, 2008;NMFS, 2017), white shrimp, in their migrations between salt marsh and offshore habitats, contribute substantially to the diets of many vertebrate and invertebrate species (Overstreet and Heard, 1978;Hettler Jr., 1989;Scharf and Schlight, 2000). In South Carolina and Georgia, U.S., white shrimp landings have decreased in recent years (NMFS, 2017), and the decline may be attributed partially to a parasitic infection directly affecting shrimp gills (Gambill et al., 2015;Frischer et al., 2017Frischer et al., , 2018. ...
... Over the past few decades, a condition known as black gill has been observed at high prevalence levels in white shrimp in the South Atlantic Bight (Gambill et al., 2015;Fowler et al., 2018), peaking in the fall with an average peak prevalence of 48% (SCDNR, unpubl.). This condition can manifest as the melanization of gill tissues as an innate immune response to gill irritants elicited across the subphylum Crustacea (Burnett and Burnett, 2015) due to a variety of pathogens, parasites, contaminants, and nutrient deficiencies (Lightner, 1985;Cerenius et al., 2010;Frischer et al., 2017). ...
... The predators used in this study typically consume prey species that are the most abundant in their environment (Llansó et al., 1998;Rosas et al., 1994), including shrimp during the summer and fall (Laughlin, 1982;Overstreet and Heard, 1982;Scharf and Schlight, 2000). In the South Atlantic Bight, black gill prevalence generally peaks during the fall (Gambill et al., 2015;Fowler et al., 2018), and high black gill prevalence could lead these and other predators to consume more shrimp than would be consumed in the absence of black gill. Such a subsidy to predators could boost their population sizes over time, while also influencing food web structure, possibly leading to further increased pressure on shrimp and other prey populations (Noonburg and Byers, 2005). ...
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.
... These symptoms are distinct and easily distinguished from general gill fouling (Figs. 1 and 2A). In contrast, the condition known as shrimp black gill, which is currently impacting penaeid shrimp populations in the Southwest Atlantic and Gulf of Mexico, is caused by a different apostome ciliate and presents as diffuse darkening of gill tissue (Gambill et al., 2015). During this study the prevalences of black spot in P. borealis during both the 2016 and 2018 sampling were estimated to be > 80% (M. ...
Black spot gill syndrome in the northern shrimp, Pandalus borealis, is caused by an apostome ciliate, Synophrya sp., found within the gill lamellae. Whole mount staining, thin section histology, electron microscopy, and molecular studies were carried out on infected gills. The Synophrya 18S rRNA from Pandalus borealis (Genbank accession no. KX906568) and from two portunid crab species, Achelous spinimanus (Genbank accession no. MH395150) and Achelous gibbesii (Genbank accession no. MH395151) was sequenced. Phylogenetic analyses confirmed the identity of these ciliates as apostomes. The 18S rRNA sequence recovered from P. borealis shared 95% nucleotide similarity with the sequences recovered from the portunid crab species suggesting that it is a different species of Synophrya. The invasive hypertrophont stages, with a distinctive macronuclear reticulum, ranged in size from 300 to 400 µm with as many as 5 large forms/mm² of gill tissue. Histotrophic hypertrophont stages and hypertomont stages were observed in these studies. The presence of the parasite was linked to the formation of melanized nodules (up to 9 nodules/mm² of gill tissue) by the host and in some cases to extensive necrosis. Other studies have reported Synophrya sp. infections in P. borealis from Greenland, Labrador and Newfoundland, but further studies are necessary to determine the prevalence of this parasite in the dense schools of northern shrimp in the North Atlantic. Questions remain as to the possibility of epizootics of this pathogen and its impact on northern shrimp populations.
... Over the past two decades, severe outbreaks of BG in penaeid shrimp have been reported off the coast of Georgia and South Carolina (Gambill et al. 2015, Fowler et al. 2018. The sBG ciliate is present in shrimp populations from approximately May through January, with peak infection rates and visibly melanized gills occurring in the late summer through the fall (August to October). ...
... Mexico although many different causative agents have been implicated (Couch 1978). In coastal Georgia and South Carolina, sBG regularly reaches high levels in the late summer and fall (Geer & Roberson 2014, Gambill et al. 2015, Frischer et al. 2017). The evidence presented here supports that gill melanization is the result of the immune response by shrimp to the presence of a large apostome ciliate that has previously been identified as the likely causal agent of sBG in the South Atlantic Bight (Frischer et al. 2017). ...
... Although the prevalence of shrimp exhibiting the symptoms of BG generally peaks in September and October (Gambill et al. 2015), the highest prevalence and intensity of sBG ciliates detected using microscopy-based approaches were observed in August (Table 1). Similar seasonal patterns have been reported with other symbiotic crustacean ciliates including the blue crabassociated peritrich ciliate Lagenophrys callinectes in Maryland Bay and the Gulf of Mexico (Couch 1983, Arias 2013. ...
Severe outbreaks of black gill (BG), heavily melanized gills of crustaceans, have been reported in white (Litopenaeus setiferus) and brown shrimp (Farfantepenaeus aztecus) from coastal Georgia and South Carolina during late summer and fall since the mid-1990s. The cause of this condition is an apostome ciliate that elicits the innate immune response of the shrimp, resulting in the formation of melanized nodules in shrimp gill tissue. In the absence of a definitive identification, the caUSAtive ciliate is referred to as the shrimp black gill (sBG) ciliate. During outbreaks, necrosis of gill tissue was often seen in microscopic sections; in some cases, there appeared to be penetration of the ciliate into gill tissue. Shrimp with BG exhibited reduced physical endurance and escape responses compared with shrimp without symptomatic BG. Physical impairment due to BG may contribute to higher predation rates and increased vulnerability to environmental conditions. The infection transmission rate of the sBG ciliate appears to be atypically low for apostome ciliates, raising the question of how epidemic levels of BG reoccur annually. Asymptomatic shrimp placed in direct contact with carcasses (heads) from BG symptomatic shrimp exhibited a significant increase in the development of BG symptoms after 7 days (P = 0.028), but waterborne transmission was not detected. A preliminary survey of sympatric crustacean species, including syntopic species of grass shrimp (Palaemonetes spp.), indicated the possible presence of the sBG ciliate, suggesting that other crustacean species may serve as infection reservoirs. These studies support the conclusion that BG is negatively impacting the penaeid shrimp fishery and highlight the challenges that remain in understanding and managing the ongoing sBG epidemic in the southeastern United States. © 2018 National Shellfisheries Association. All rights reserved.
... In aquaculture settings, ascorbic acid deficiency is also known to evoke black gill in penaeid shrimp (Magarelli et al. 1979). Since the early 2000s, there has been an ongoing epidemic of shrimp black gill (sBG) in wild penaeid shrimp populations along the southwestern Atlantic coastal zone with its epicenter off the coasts of Georgia and South Carolina (Gambill et al. 2015). The primary species that have been affected are Litopenaeus setiferus (white shrimp) and Farfantepenaeus aztecus (brown shrimp). ...
... Shrimp black gill is well established in wild penaeid shrimp populations in the southeastern Atlantic and Gulf of Mexico although many different causative agents have been implicated (Couch 1978). In coastal Georgia and South Carolina, sBG regularly reaches high levels in the late summer and fall (Geer 2013, Gambill et al. 2015. The cause and consequences of this condition, however, are poorly understood. ...
Penaeid shrimp including Litopenaeus setiferus (white shrimp), Farfantepenaeus aztecus (brown shrimp), and Farfantepenaeus duorarum (pink shrimp) support one of the most valuable commercial fisheries in the U.S. Southeast Atlantic. Since the late 1990s, the fishery, especially in coastal Georgia and South Carolina, has experienced a significant decline. A contributing factor to this decline has been hypothesized to be a severe outbreak of shrimp black gill caused by a ciliate parasite. DNAsequence-based analysis of the gill parasite small subunit rRNA gene identifies the proposed causative agent as being closely related to the apostome ciliate Hyalophysa chattoni; however, morphological characteristics of the ciliate observed by electron microscopy are inconsistent with this identification. Although studies are ongoing to identify this ciliate, it was possible to develop a diagnostic polymerase chain reaction-based assay targeting the small subunit rRNA gene and use it to investigate the seasonal and geographic distribution of the parasite in wild shrimp populations. Next-generation sequencing of the gill microbiome confirmed that when black gill is at its peak, microeukaryotic communities were dominated by apostome-related ciliates, but over the year highly diverse communities of gill associates, including other potential ciliate, fungal, euglenozoid, and amoeboid parasites are commonly detected. Improved molecular diagnostics and the ability to explore the diversity of potential parasites in shrimp provide important new insights into the relationship between the shrimp fishery and black gill.
Student Assignment (Ph.D Course)
The parasitic ciliate causing shrimp black gill (sBG) infections in penaeid shrimp has been identified. The sBG ciliate has a unique life cycle that includes an encysted divisional stage on the host's gills. The ciliature of the encysted trophont stage has been determined and is quite similar to that of the closely related apostomes Hyalophysa bradburyae and H. chattoni. Hyalophysa bradburyae is a commensal ciliate associated with freshwater caridean shrimp and crayfish, while H. chattoni is a common commensal found on North American marine decapods. Based on 18S rRNA gene sequence comparisons, the sBG ciliate is more closely related to the marine species H. chattoni than to the freshwater species H. bradburyae. The unique life cycle, morphology, 18S rRNA gene sequence, hosts, location, and pathology of the sBG ciliate distinguish this organism as a new species, Hyalophysa lynni n. sp.
