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Probopyrus pandalicola: Discontinuous ingestion of shrimp hemolymph
Abstract
Grass shrimp, Palaemonetes pugío, were injected with 14C-labelled amino acids to determine hemolymph losses caused by an ectoparasite, the isopod Probopyrus pandalícola (Packard) (Epicaridea; Bopyridae). The female parasites were removed from labelled shrimp at intervals over 36 hr to monitor hemolymph ingestion. The parasites were found to feed discontinuously throughout the host's molt cycle, ingesting an average of 7–9 μl of hemolymph over a 24-hr period. Feeding was curtailed in darkness; probopyrids consumed only 2–3 μl of hemolymph after 12 hr in the dark. In all experiments, a number of parasites did not feed. The results of this study indicate that significant losses of the host's hemolymph result from the feeding activity of P. pandalicola. The determination of these losses is essential to begin testing the hypotheses that losses of hemolymph inhibit gonadogenesis in the host by either (i) creating a nutrient imbalance or (ii) depleting titers of reproductive hormones.
... Parasitic interactions among isopods and prawns are common and reasonably well known in the scientific literature, mainly given that many parasitic isopods are crustacean specific and feed on their hemolymph (Walker 1977;Boxshall et al. 2005). More specifically, ectoparasitic isopods from the family Bopyridae usually infect prawns as their definitive hosts and remain attached to their branchial chambers until it dies (Beck 1980b;Chaplin-Ebanks and Curran 2007), mainly because of the capacity of the female isopod to avoid being released along with the old exoskeleton by instantly latching onto the new structure, allowing the parasite to grow along with its host (Cash and Bauer 1993). ...
... More specifically, our results suggested that parasitized individuals grew much slower because they had the relationship between carapace length (CL) and total length (TL) altered, as represented by the equation parameters in the Fig. 5. This can possibly be a result of the haemolymph loss caused by the feeding of the parasite (Walker 1977). The subsequent loss of nutrients caused by it can disturb and inhibit the synthesis of hormonal compounds that are thought to stimulate maturation processes (Fingerman 1997;Subramoniam 2011;Swetha et al. 2011). ...
... It is mainly acknowledged on the limitation of the host's movements (e.g. foraging/looking for resources, directly linked to energy gains) (Ghai et al. 2015), energetic outcomes of fighting the parasites back (even though that evidence in the scientific literature for immunity expenses are so far blended) (Bonneaud et al. 2003;Eraud et al. 2005;Nilsson et al. 2007), environmental factors that can lead to increased probability of transmission such as resource scarcity (Ostfeld et al. 2005;Becker et al. 2015) and fluid loss (Walker 1977;Smith et al. 2008). Particularly, in the studied shrimp, it is more likely that the relative contribution of fluid loss and limitation of movements are far more important in explaining the worsened nutritional condition, since the loss of haemolymph in crustaceans are commonly linked to nutrient loss and limitation of movements can modify feeding behaviours and also provide an important diminution of nutrient intake (Felten and Guerold 2001;Lester 2005). ...
In this study, we aimed to record, for the first time, parasitic infestation by the isopod Probopyrus pan-dalicola on the prawn Macrobrachium acanthurus, as well as to register some ecological interactions. We hypothesized that the parasitic infection is able to negatively affect the prawn's nutritional condition and that this interaction can modify growth relationships in male individuals. We collected both parasitized (n = 25) and parasite-free (n = 25) individuals in several locations of the Contas River, state of Bahia, Brazil, which had their morphometric characteristics determined, including of the parasites. Relative growth models were constructed for both groups in order to compare slopes and intercepts and determine if the growth patterns are modified by the parasite. We also determined the body condition of the prawns, which was also compared between the two groups. Our results clearly demonstrated that the parasitic infection is able to induce modifications in relative growth patterns in male individuals and that this isopod is capable of reducing the nutritional condition of the prawns. This study indicates that this parasite can induce deleterious effects in the prawn, but individually. Further studies should be conducted to assess the relevance of our findings in conservation and management.
... Adult bopyrids are typically found in female-male pairs (Anderson, 1990), either within the branchial chamber or on the abdomen of their hosts (Reinhard, 1956;Markham, 1985). Bopyrids negatively affect their definitive hosts in several ways, including decreased growth (Van Wyk, 1982;Jay, 1989;Ludwig, 2009), reduced energetic reserves (Neves et al., 2004;Repetto and Griffen, 2011), and loss of hemolymph (Walker, 1977). Some authors found that bopyrid isopods also lower the activity level of their shrimp hosts (Bass and Weis, 1999;McGrew and Hultgren, 2011);however, Chaplin-Ebanks and Curran (2005) determined that the activity level of shrimp parasitized by bopyrids was not significantly different from that of unparasitized shrimp. ...
... Probopyrus pandalicola is a bopyrid isopod that infects several palaemonid shrimp species, including the daggerblade grass shrimp Palaemonetes pugio (Anderson, 1977;Walker, 1977;Markham, 1985;Kensley and Schotte, 1989;Cash and Bauer, 1993;Chaplin-Ebanks and Curran, 2005), which is abundant in estuaries along the East Coast of the United States and in the Gulf of Mexico (Sikora, 1977;Kneib, 1985). Anderson (1977) found that 3.0% of Palaemonetes pugio were parasitized by Probopyrus pandalicola in North Inlet estuary in Georgetown, South Carolina. ...
... Bopyrid hosts may be unable to reproduce because the parasite possibly secretes or causes the secretion of a gonad-inhibiting hormone (Beck, 1980b). A potential decrease in the reproductive hormones of the host as a result of hemolymph loss caused by the parasite (Walker, 1977) could also be a factor. Beck (1980b) stated that the simplest reason for the sexual sterilization of females is host energy depletion caused by the parasite. ...
Abstract Probopyrus pandalicola is a bopyrid isopod that infects several palaemonid shrimp species, including the daggerblade grass shrimp Palaemonetes pugio. The parasite can have several negative effects on its host, including loss of hemolymph, reduced reproductive potential, and decreased molting frequency and growth. To date, there are conflicting reports on whether Probopyrus pandalicola affects the reproductive capability of both male and female daggerblade grass shrimp. The purpose of this study was to determine whether infection by Probopyrus pandalicola resulted in the sexual sterilization of Palaemonetes pugio, and if the reproductive capability of male and/or female shrimp was restored after the bopyrid was removed. We found that parasitized and deparasitized males were able to successfully fertilize the eggs of unparasitized females, as 18.9±7.1% and 42.7±5.2% of the females paired with them became ovigerous in 4 wk, respectively. Neither parasitized nor deparasitized females became ovigerous when placed with unparasitized males during the 4-wk period. However, 45.4±20.6% of deparasitized females did become ovigerous within 10 wk. Despite the fact that female shrimp are able to reproduce when no longer parasitized, the majority of females remain infected with the bopyrid for their entire lives. Therefore, the sexual sterilization of female shrimp could potentially have a significant impact on estuarine food webs, as grass shrimp are conduits of detrital energy and a food source for many recreationally and commercially important species in estuaries on the East Coast of the U.S.A. and in the Gulf of Mexico.
... Few data are available regarding the effects of parasitism on hostreserve mobilization during energetic deprivation and/or expenditure, and also regarding the parasite's energetic reserves during host starvation. Therefore, considering the above facts, as well as the information that bopyrid isopods can consume up to 80 µl d –1 of host hemolymph (Walker 1977), our aim was to study how parasitism by Probopyrus ringueleti affects energetic reserve utilization by P. argentinus during starvation, through determinations of glucose, glycogen and total lipid concentrations. This work also aimed to verify, for the first time, the effects of host starvation on bopyrid energetic reserves. ...
... Some parasitic helminthes display similar responses but without restoration of energetic reserves, except when starvation is suspended (Halton 1997). According to Walker (1977), circulating nutrients in the host may regulate the ingestion of hemolymph by ectoparasitic isopods, and the reduction in circulating nutrients could decrease parasite hemolymph ingestion and/or stimulate the utilization of their own reserves. Indeed, hormonal factors that initiate glycogenolysis or beta-oxidation pathways in hosts could have a similar metabolic effect on the parasite. ...
... Indeed, hormonal factors that initiate glycogenolysis or beta-oxidation pathways in hosts could have a similar metabolic effect on the parasite. In this way, isopod metabolism appears to be dependent on the processes which regulate their hosts' metabolism or, at least, they are rapidly influenced by the host hemolymphatic nutrient concentrations , as predicted by some early authors (Veillet 1945, Hartnoll 1967, Field 1969, Walker 1977). The similar pattern of reserve utilization found in isopods and their host shrimp, when the isopods have had normal access to host nutrients, suggests parasite metabolic dependency on host regulatory mechanisms. ...
Effects of the branchial ectoparasite isopod Probopyrus ringueleti on the utilization of glucose, glycogen and total lipids on starved shrimp Palaemonetes argentinus were evaluated, as well as the isopod responses to host starvation. Shrimp were maintained for 12 d under laboratory conditions. Parasitized and unparasitized shrimp were starved for 15 d, and glucose, glycogen and total lipid concentrations were determined at 0, 24, 72, 168 and 360 h of starvation. During starvation, control animals (unparasitized) preferentially metabolized lipids and preserved their carbohydrate reserves. Parasitized shrimp had lower lipid concentrations than unparasitized shrimp, and preferentially metabolized carbohydrates. Bopyrids displayed a similar response, with glycogen depleted at the beginning of the starvation period followed by subsequent reestablishment. Our results demonstrated that bopyrids affect host energy allocation. The lower initial lipid concentration of parasitized shrimp suggested that the host is disadvantaged from both food deprivation and isopod nutritional demands. A possible dependency of P. ringueleti on the mechanisms that control host metabolic processes was also suggested.
... The term parasitic castration can be used loosely however. It does not always refer to the direct destruction or devouring of the host's gonads, but can also be the indirect result of a nutritional drain or hormonal interference by the parasite (Baudoin, 1975;Walker, 1977;Van Wyk, 1982;Coustau et al., 1991). Most of the time there is very little or no physical damage done to the gonads (Baudoin, 1975). ...
... He argued that the partial castrator phenomenon seemed most consistent with the nutritional drain hypothesis. If it is likely that energy ingestion rates such as those observed by Anderson (1977) and Walker (1977) in shrimp parasitized by bopyrids can affect crustacean fecundity on a number of levels, then comparable energy ingestion rates of A. apogonae on C. quinquelineatus could theoretically produce the same outcome. Sub-optimal nutrition in parasitized C. quinquelineatus could also explain the retarded growth rates compared to unparasitized fish, as was proposed for the porcellanid crab Pachycheles rudis infested with the bopyrid isopod, Aporobopyrus muguensis (Van Wyk, 1982). ...
A thesis submitted for the degree of Master of Philosophy at The University of Queensland in August 2005.
... Two hypotheses that have rarely been explored might explain host castration by pea crabs. First, the 'energy drain' hypothesis proposes that parasitic castrators, such as pea crabs, cause host reproductive cessation by depleting energy reserves from host individuals due to food deprivation and/or damage of tissues imposed by these parasites (Walker 1977;Van Wyk 1982;Hurd 1993;Polak 1996). This first hypothesis appears to explain castration in insects infested by parasitic mites (Polak 1996) and crabs harboring parasitic isopods (Van Wyk 1982) and might also explain the absence of reproductive activity in bivalve hosts infested by pea crabs. ...
... Two hypotheses might explain the observed reproductive cessation in infested limpets. First, the 'energy drain' hypothesis proposes that parasitic castrators, such as C. garthi, cause reproductive cessation by depleting energy reserves from host individuals due to food diversion and/ or damage of tissues imposed by these parasites (Walker 1977;Van Wyk 1982;Polak 1996). alternatively, reproductive cessation of infested limpets might be simply due to the physical presence of crabs within hosts that interferes with (inhibits) reproduction, as reported in the pea crab Calyptraeotheres sp. and the slipper limpet Crepipatella fecunda from the southeastern Pacific (Chaparro et al. 2001). ...
Two ill-explored hypotheses might explain host castration by parasitic pea crabs. The 'energy drain' hypothesis states that castration is caused by host-derived nutrient consumption of parasites that ultimately diminishes host-energy intake. The 'steric interference' hypothesis states that castration occurs when parasites physically inhibit host reproduction. This study evaluated whether Calyptraeotheres garthi, a pea crab from the southwestern Atlantic, is a parasitic castrator and explored whether the two hypotheses above explain castration in the limpet Crepidula cachimilla. None of three studied limpet species brooded embryos during the reproductive season when infested by mature female pea crabs. Also, limpets of C. cachimilla infested by C. garthi did not reproduce during a 90-day experimental period while crab-free limpets did spawn embryos during this period. Limpets resumed reproduction soon after pea crabs were experimentally removed from their brooding chamber. Thus, C. garthi does castrate limpets, and castration is reversible. Pea crabs 'steal' food from limpets, and infested limpets did not modify their feeding behavior to counteract nutrient loss. Thus, infested limpets are expected to ingest less food which provides partial support for the 'energy drain' hypothesis. However, the limpet's body condition increased or was not affected by pea crabs during the breeding season which argues against the same hypothesis. Furthermore, that limpets promptly recovered reproductive activity once pea crabs were experimentally removed, that castration was not induced by the smallest pea crabs in the population (that fill only partially the brooding chamber), and that parasitized limpets did exhibit fully mature ovaries, support the 'steric interference' hypothesis explaining parasitic castration.
... Es posible que este oriHcio pehnita la succi6n de hemoUnfa, de la cual el isopodo se alimenta. Este tipo de alimentacidn se estableci6 para Munidion initans Boone, 1927 (Bursey, 1978) y para Probopyrus pandalicola (Padcard, 1879) (ver Walker, 1977;Bursey, 1978). El macho se encontr6 sujeto a la primer pata caminadora dcrecha y no es frecuente encontrarlo sobre la superficie ventroabdominal de la hembra (Richardson, 1905 of the isopod mouth parts were introduced in the middle of the protopodite. ...
... It is possible that this orifice allows suction of hemolimph on which the female isopod feeds. This mode of feeding has been established for Munidion initans Boone, 1927 and for Pmbopyrus pandalicola (Packard, 1879) (see Walker, 1977;Bursey, 1978). The male was found attached to the first right walking leg and its uncommon on the ventroabdominal surface of the females (Richardson, 1905 Remarks.* ...
... The energetics of marine bopyrid isopods are poorly known due to the low prevalence of these parasites, their complex life history, and the difficulties experienced in culturing them in the laboratory. Walker (1977) traced radioactive amino acids in the brackish water grass shrimp, Palaemontes pugio, and estimated that this host loses up to 25% of its hemolymph volume daily to the bopyrid Probopyrus pandalicola. Anderson (1977), compared oxygen flux rates in P. pugio infested by P. pandalicola and estimated that 10% of daily energy intake by P. pugio was lost to the parasite. ...
... Anderson (1977), compared oxygen flux rates in P. pugio infested by P. pandalicola and estimated that 10% of daily energy intake by P. pugio was lost to the parasite. O'Brien and van Wyk (1985) reanalyzed the data of Walker (1977) and Anderson (1977), and concluded that bopyrids ingest 4.3-4.4% of the daily energy intake of their hosts and this energy loss is equivalent to the energy devoted to reproduction in non-parasitized shrimp. We did not estimate rates of energy uptake. ...
The population structure and energetic burden of bopyrid isopod parasite Orthione griffenis on the eastern Pacific mud shrimp Upogebia pugettensis are estimated from size and weight relationships between parasite and host. U. pugettensis weight loss increases with O. griffenis weight but the high variance in the relation indicates that direct weight comparisons are insufficient to reveal most of the host-parasite energetic interactions. Environment, reproductive development, age, molt stage and the feeding histories of the hosts and parasites, not apparent from weight ratio comparisons, are likely to be important factors in their interaction. The high prevalence of O. griffenis among U. pugettensis and positive correlation between host weight loss and parasite weight nevertheless, indicate large impacts of these parasites on mud shrimp populations are occurring with corresponding effects on estuarine dynamics in Pacific Northwest estuaries.
... P. pugio's overall lifespan ranges anywhere from 6 to 13 months and adults may reach a maximum size of up to 50 mm (Alon and Stancyk, 1982). Probopyrus pandalicola (Packard) (Epicaridea; Bopyridae) is a hematophagous ectoparasitic isopod that infests palaemonid shrimps, including P. pugio (Pike, 1960; Walker, 1977; Cash and Bauer, 1993). Based primarily on observations of field-collected adult hosts, some studies concluded that the vitality of infected hosts is unimpaired (Morris, 1948; Van Wyk, 1982). ...
... his study as well as ours, P animals captured either fewer or an equal amount of prey, but not more. If parasitized shrimp have lower (or equal) prey capture, and decrease their feeding activity disproportionately after observing a predator they can incur energetic deficits, since the metabolic demands of the parasite are added to the host's needs. Walker (1977) estimated that a parasitized grass shrimp lost up to 25% of its hemolymph volume daily to the isopod. Anderson (1977) estimated that up to 10% of the daily energy intake of P. pugio went to the bopyrid. Thus, the isopods are a significant energy drain for the shrimp. The lower activity level of P shrimp in the glass tank, (when not resp ...
Preliminary observations indicated that the grass shrimp, Palaemonetes pugio, parasitized by the isopod, Probopyrus pandalicola, captured significantly fewer prey items (Daphnia) and exhibited reduced activity compared to unparasitized conspecifics. Further research focused on elucidating the factors involved in altering the shrimp’s behavior. When viewed from above in an opaque container, activity levels of parasitized shrimp were considerably lower than unparasitized shrimp; however, when viewed from the side in a glass container, differences in activity were also seen, but not under all circumstances. In response to the observer above, the parasitized shrimp reduced their activity disproportionately. When (in the opaque tank) prey capture of Artemia was examined, there was no difference between parasitized and unparasitized shrimp’s capture rate. This is attributable to the greater activity of Artemia, which makes them more likely than Daphnia to encounter a relatively inactive predator. There was not a significant difference in prey capture when Cyprinodon larvae were used as prey and tanks were not observed from above. When predator avoidance was studied using mummichogs (Fundulus heteroclitus), we expected that the more conspicuous parasitized shrimp would be preyed upon more, but this was not the case. Their lowered activity in the presence of a predator apparently reduced their conspicuousness, so that they were not preyed on more than the unparasitized shrimp.
... Since host and parasite endocrinology is still insufficiently known, energy drain and/or endocrine disruption have been suggested to be the mechanism responsible for the occurrence of parasitic castration. Increased nutritional demand by the parasite significantly affects PS energy flow as a result of consumption of host hemolymph and nutrient imbalance (Rein- Anderson 1977, Walker 1977, and may be enough to impair the production of energetically costly vitellogenic oocytes. With regards to endocrine disruption, parasites may deplete titers of reproductive hormones, stimulate the production of the gonad-inhibiting hormone (GIH) or even secrete GIH (Baudoin 1975, Walker 1977, Beck 1980. ...
... Increased nutritional demand by the parasite significantly affects PS energy flow as a result of consumption of host hemolymph and nutrient imbalance (Rein- Anderson 1977, Walker 1977, and may be enough to impair the production of energetically costly vitellogenic oocytes. With regards to endocrine disruption, parasites may deplete titers of reproductive hormones, stimulate the production of the gonad-inhibiting hormone (GIH) or even secrete GIH (Baudoin 1975, Walker 1977, Beck 1980. The different degrees of inhibition of the female function owing to bopyrid isopods (total in the case of abdominal parasites and partial in that of branchial parasites) currently detected in the genus Lysmata may be accounted for by the relative larger size of abdominal parasites, which may drain more energy or disrupt endocrine mechanisms more severely than branchial bopyrids. ...
This study evaluates possible parasitic castration induced by a bopyrid isopod of the genus Parabopyrella, which parasitizes the branchial chamber of the simultaneously hermaphroditic shrimp Lysmata amboinensis. Parasitized shrimp (PS) carried embryos and produced significantly fewer larvae (mean +/- SD: 363 +/- 102; p = 0.002) than formerly parasitized shrimp (FPS) (1297 +/- 143) and unparasitized shrimp (US) paired with other US (1409 +/- 102), with PS (1362 +/- 234) or with FPS (1384 +/- 157). Starvation trials revealed no significant differences in the quality of larvae produced by PS, FPS and US paired with other US, PS and FPS. Host embryo production is only quantitatively, not qualitatively, affected, probably due to nutritional drain and/or endocrine disruption caused by the parasite. The host male sexual system remains fully functional and 'reproductive death' does not occur. The feminization of pleopods that prevents parasitized males of gonochoric species from successfully copulating seems to have no effect on L. seticaudata: pleopods are always feminized during their transition from male to simultaneous hermaphrodite phase, with adults being able to successfully fertilize broods. Parabopyrella sp. significantly affects the female sexual system of its host, but does not cause castration, as recorded for L. seticaudata parasitized by the bopyrid isopod Eophryxus lysmatae (an abdominal parasite).
... Ectoparasitic isopods from the family Bopyridae usually infect prawns as their definitive hosts and remain attached to the prawns' branchial chambers (Beck, 1980;Chaplin-Ebanks & Curran, 2007). Parasitic interactions between isopods of Bopyridae and prawns are common and reasonably well known in the scientific literature, mainly because many parasitic isopods are crustacean-specific and feed on their hemolymph (Walker, 1977;Boxshall et al., 2005). This happens in many species of the genus Macrobrachium (Collart, 1990;Román-Contreras, 1996;Masunari et al., 2000;Conner & Bauer, 2010;Vargas-Ceballos et al., 2016). ...
The Amazon prawn or Macrobrachium amazonicum (Heller, 1862) is widely distributed in South America, occurring in the Orinoco and Amazon rivers, and forms an important source of income for riverside families. This prawn hosts crustacean ectoparasites of the genus Probopyrus (Giard & Bonnier, 1888) (Bopyridae) that infest its gill cavity. The aim of the present study was to report new occurrences of Probopyrus in Amazon prawns caught in the Amazon River. Macrobrachium amazonicum prawns were collected between May 2017 and April 2018, and again from July 2021 to May 2022 in the regions of Ilha de Santana and Rio Mazagão, state of Amapá, Brazil. Among the 5,179 prawn specimens caught, 133 were parasitized by the ectoparasites Probopyrus pandalicola (Packard, 1879), Probopyrus bithynis (Richardson, 1904), Probopyrus floridensis (Richardson, 1904) and Probopyrus palaemoni (Lemos de Castro & Brasil Lima, 1974). These occurrences of P. floridensis and P. palaemoni in M. amazonicum were the first records of this on the northern coast of Brazil. These four ectoparasites are not limited to specific host species or genera, as observed in this study, which reports four species of Probopyrus infesting M. amazonicum.
... Parasitism by epicaridean isopods poses a metabolic drain on the decapod host because female parasite individuals feed on host hemolymph and ovarian fluids after piercing the host's cuticle (Bursey 1978;Lester 2005). For example, a bopyrid parasite can consume up to 25% (Anderson 1977;Walker 1977) of hemolymph volume per day, for a species of carid shrimp. Consequently, a lower growth rate leading to smaller average and maximum sizes within parasitized specimens may be expected. ...
The fossil record of crustaceans as hosts of parasites has yielded three confirmed associations: swellings on Jurassic–Pleistocene decapods attributed to epicaridean isopods, feminization of Cretaceous and Miocene crabs possibly caused by rhizocephalan barnacles, and presumed pentastomids on/in Silurian ostracods. Cestode platyhelminth hooks and swellings by entoniscid isopods have yet to be recognized. Relative to 2014, we report a 45% increase to 128 fossil decapod species with swellings (ichnotaxon Kanthyloma crusta) in the branchial chamber attributed to epicarideans. Furthermore, using a Late Jurassic decapod assemblage from Austria, we find (1) no correlation between genus abundance and prevalence of K. crusta, (2) host preference for some galatheoids (as for a mid-Cretaceous assemblage from Spain), and (3) a larger median size of parasitized versus non-parasitized specimens for two abundant species. The latter result may be caused by infestation throughout ontogeny rather than exclusively in juveniles and/or possible selection for larger individuals.
... Among the changes caused by parasitism in this species, the size reduction of the male chelipeds and female abdomens can be regarded as developmental inhibition caused by nutrient depletion (Walker, 1977). However, the presence of short female-like setae on male chelipeds (Fig. 2 N,O) and the size enlargement of the male abdomen cannot be explained by passive developmental defects, but by active developmental/physiological regulations such as hormonal actions (Beck, 1980;Calado et al., 2006). ...
Although many animals that perform sexual reproduction exhibit sexual dimorphism, individuals with intersex traits between the traits of males and females appear in some species, depending on environmental factors. Ptychognathus ishii, a varunid crab, exhibits distinctive sexual dimorphism in the morphology of its abdomen, chelipeds and setal tufts on the chelipeds. In this study, however, we report for the first time that intersex individuals with intermediate characters between those of males and females were occasionally found in wild populations. Morphological features of intersex individuals are described. Their taxonomic positions are identified based on DNA sequences of part of the mitochondrial cytochrome c oxidase I (COI) gene. It was shown that the intersexuality was induced by entoniscid parasites, because all intersex individuals were parasitized by entoniscid isopods, identified as Entionella sp. The apparent correlation between parasitism and morphological anomalies suggests that the parasitic isopods affect physiological conditions, leading to the feminization of male hosts.
... Parasitism by epicaridean isopods poses a metabolic drain on the decapod host because female parasite 301 individuals feed on host hemolymph and ovarian fluids after piercing the host's cuticle (Bursey 1978;302 Lester 2005). For example, a bopyrid parasite can consume up to 25% (Walker 1977) ...
The fossil record of crustaceans as hosts of parasites has yielded three confirmed associations: epicaridean isopod-induced swellings on Jurassic-Recent decapod crustaceans, feminization of Cretaceous and Miocene male crabs possibly caused by rhizocephalan barnacles, and presumed pentastomids on/in Silurian ostracods. Cestode platyhelminth hooks and swellings by entoniscid isopods may be recognized in the future. Relative to 2014, we report an increase of 41% to 124 fossil decapod species with epicaridean-induced swellings in the branchial chamber (ichnotaxon Kanthyloma crusta). Furthermore, using a Late Jurassic (Tithonian) decapod assemblage from Austria, we find (1) no correlation between genus abundance and prevalence of K. crusta, (2) host preference for some galatheoid taxa (as for a mid-Cretaceous assemblage from Spain), and (3) a larger median size of parasitized versus non-parasitized specimens for two selected species. The latter result may be caused by infestation throughout ontogeny rather than exclusively in juveniles and/or possible selection for the larger sex.
... If nutrition derived from the host or the ability of a P. lata female to acquire food from its host diminishes with increased parasite size, small but not large females might have access to enough resources to produce and accumulate yolk entirely filling their body cavities. Unfortunately, little is known about how bopyrid isopods derive nourishment from their hosts (Walker 1977;Astete-Espinoza and Caceres 2000;Neves et al. 2004), so future studies are needed to understand if nutrition becomes limiting for large females. ...
Knowledge of marine host–parasite relationships has been increasing, but little is known about the reproductive strategies of the parasites. Theoretically, parasitic crustaceans inhabiting relatively small and scarce hosts should be monogamous. Parasites are also expected to exhibit higher reproductive performance (RP) than their free-living relatives, a strategy thought to have evolved to increase host-to-host transmission, or to be the outcome of living in a ‘stable, nutrient-rich environment’. Here, the parasitic isopod Parabopyrella lata and its shrimp host Lysmata boggessi were used to test for monogamy and augmented RP, and to examine whether or not P. lata castrates its host. Prevalence, population distribution, and reproductive performance were examined in P. lata over 1 year (2012–2013) off Homosassa Springs, Florida USA (28.8037° N, 82.5761° W). Prevalence of P. lata on L. boggessi was greater during the warmer months of the year and infested shrimps were almost exclusively males. P. lata lives in male–female pairs within the gill chamber of infested shrimps more frequently than expected by chance alone. The sizes of paired males and females were tightly and positively correlated with each other and with host size. Average fecundity (3660 ± 1146 eggs female⁻¹) and reproductive output (61 ± 19%) in P. lata, as with other bopyrid parasites, was much greater than those reported for free-living isopods. This evidence supports the hypotheses that parasites such as P. lata are adapted to be monogamous, display augmented RP, and reproductively castrate their host.
... Cette réduction résulte du fardeau énergétique que représente le parasite puisque sa demande métabolique s'ajoute à celle de son hôte. Il a d'ailleurs été estimé que P. pandalicola ingère quotidiennement jusqu'à 25 % du volume total de l'hémolymphe de P. pugio (Walker, 1977), induisant ainsi une demande énergétique qui représente jusqu'à 10 % des besoins quotidiens de l'hôte (Anderson, 1977). Dans le cas des thalassinidés, la relation hôte-parasite pourrait avoir d'importantes répercussions sur le fonctionnement des écosystèmes si le bopyre affecte un trait impliqué dans un processus responsable du caractère ingénieur de l'hôte (Thomas et al., 1999). ...
Dans le bassin d’Arcachon, le crustacé thalassinidé Upogebia pusilla habite préférentiellement les vasières intertidales colonisées par les zostères naines (Zostera noltei) où il trouve la stabilité sédimentaire indispensable à l’établissement durable de son terrier. Du fait de la profondeur de ce dernier (> 30 cm) et de sa grande mobilité, cette espèce ingénieure a souvent été négligée dans les études antérieures ayant pour objectif de mieux comprendre le rôle des communautés macro-benthiques dans le fonctionnement des herbiers de phanérogames et les conséquences de leur régression rapide. Ce manuscrit présente une étude intégrée du rôle d’U. pusilla dans le fonctionnement de son écosystème en s’attachant particulièrement à caractériser et quantifier les relations entre (1) ses différentes activités (fouissage, ventilation, locomotion, …), (2) les modes de bioturbation qui en résultent et (3)leurs impacts respectifs sur la dynamique biogéochimique sédimentaire. Ce travail montre qu’U. pusilla engendre un remaniement et une bioirrigation intenses de la matrice sédimentaire qui l’entoure. Sa présence stimule ainsi fortement la reminéralisation de la matière organique sédimentée et les échanges de solutés à travers l’interface eau-sédiment.Bien que l’influence d’U. pusilla sur ces processus écologiques et biogéochimiques soit très dépendante des conditions environnementales (e.g., saisonnalité, prévalence parasitaire),l’ensemble de mes résultats suggère que le déclin progressif de ses populations, conséquence directe de la dégradation de son habitat, est susceptible de fortement altérer le fonctionnement global des écosystèmes du bassin d’Arcachon.
... Gonads of infected fish, however, were hardly visible. The mechanism of parasitic castration of the host remains poorly known, but hormonal interference (Beck, 1980;Lima et al., 2007) and nutritional drain caused by the parasite (Anderson, 1977;Walker, 1977;Conner & Bauer, 2010) have been proposed as explanations. Another cymothoid isopod, Riggia paranensis Szidat, 1948, which burrows into the flesh of its fish host, Cyphocharax gilbert Quoy & Gaimard, 1824, also causes parasitic castration (Azevedo et al., 2006). ...
A total of 336 specimens of the goldfish Carassius auratus Linnaeus, 1758 were examined in the Baihe River, Henan Province, China, for the presence of the parasitic isopod Ichthyoxenus japonensisRichardson, 1913. Only 20 goldfish (5.95%) were infected with single and paired isopods, and seven fish were previously infected. There was no significant difference in mean body condition (as K = (EW/L³) × 100, where EW is the eviscerated body weight and L is fork length) between infected (mean 1.450) and uninfected fish (mean 1.448; P = 0.95). The weight of gonads of the infected fish (N = 20) was calculated as zero because the gonads were too small to weigh or to identify the sex. There was also no significant difference in the GSI (gonadosomatic indices) between the infected fish (mean 2.66) and the uninfected individuals (mean 4.80; P = 0.30). The results suggest that the reproductive ability of the host was severely reduced by infection of the isopod, but that the gonads of the castrated fish could recover after the loss of the isopods.
... Females of bopyrids appear to suck large amounts of hemolymph from their hosts. Walker (1977) estimated that about a 25% of the hemolymph of Palaemonetes pugio Holthuis, 1949, is taken daily by Probopyrus pandalicola (Packard, 1879). The mature female of L. distorta punctures a large vessel of U. uruguayensis, which most likely provides abundant hemolymph for the parasite (see Roccatagliata and Torres Jordá, 2002). ...
On the basis of a sampling program performed monthly, a total of 12,033 fiddler crabs, Uca uruguayensis, were collected at the southern end of the Samborombon Bay, Rio de la Plata estuary, Argentina, from February 1995 to March 1996. Density ranged from 133 to 207 ind/m2 over the 13-mo study period. The overall proportion of male crabs was 0.62. For small crabs, sex ratio was 1:1, but as crab size increased, sex ratio first became female biased and then male biased. Crabs carried eggs from mid-spring to late summer. Prevalence of the parasite Leidya distorta varied between 5.24% and 17.8% throughout the study. Infested male crabs ≥10.5 mm carapace width, which represented only 5.9% of the crabs collected, housed 68.8% of the total parasites recovered. Cryptoniscus larvae were much more frequent among molting (soft) than intermolt (hard) crabs. The cryptonisci infesting intermolt (hard) crabs were aggregated; i.e., they showed a contagious distribution. Females of L. distorta were actively breedin...
... Castration of crustacean host has been suggested as nutritional drain by the parasite and secretion of toxic substance (Cencig et al., 2013;Reinhard, 1956), reduction in circulating reproductive hormones (Robert, 1997;Lafferty and Kuris, 2009;Walker, 1977), indirect hormonal castration (Hechinger, 2010;Baudoin, 1975) or in male host, decline of secretion by the androgenic gland (Chariniaux-Cotton, 1960). Castrators may use advantage by the reduction of host reproductive efforts by the sense of increased host survivorship (Shawal et al., 2008;Caladona et al., 2005;Wecker, 1962); increased host growth (Calado et al., 2005;Cheng, 1971) and increased energy availability (Hughes, 1940). ...
A B S T R A C T
Parasite of Charybdis feriatus has been identified as Micippion asymmetricus Shiino (1942) on the
basis of epicraidean larvae’s 6th pareopod size and shape. Parasitic castrator retards the development
of the gonads or destroys sex cells resultant complete atrophy in Charybdis feriatus. Infestation (5%)
appears as biological limiting factor which causes fluctuation in Charybdis feriatus abundance.
Infestation in C. feriatus observed throughout the year except August and December. Maximum
number of infestation recorded in January with 10 individuals and minimum in February and it effect
on their growth, gonad development as well as on population. Among deep sea crabs C. feriatus
stand first in high fecundity but their population ranked after P. pelagicus and P. sanguinolentus in
Karachi waters. Charybdis feriatus is widely distributed throughout the Indo-Pacific region and is
fished for human consumption. The crab has very good market potential but more knowledge is
required of its basic biology and ecology.
... Bopyrid isopods cause blood loss and effectively castrate their decapod crustacean hosts (Kuris 1974;Walker 1977;O'Brien and Van Wyk 1985), but are not expected to cause mortality. Since U. pugettensis is likely a novel host for O. griffenis and some bopyrids are not full castrators, we wanted to verify this relationship for this host/parasite system. ...
... Female bopyrids feed with stylet-like mandibles that pierce the inner wall of the branchiostegite to suck hemolymph from their hosts (Walker, 1977). The mature female of L. distorta punctures a large horizontal vessel of U. uruguayensis before this vessel enters the pericardial sinus. ...
On the basis of a sampling program performed monthly, a total of 12,033 fiddler crabs, Uca uruguayensis, were collected at the southern end of the Samborombón Bay, Río de la Plata estuary, Argentina, from February 1995 to March 1996. Density ranged from 133 to 207 ind/m2 over the 13-mo study period. The overall proportion of male crabs was 0.62. For small crabs, sex ratio was 1:1, but as crab size increased, sex ratio first became female biased and then male biased. Crabs carried eggs from mid-spring to late summer. Prevalence of the parasite Leidya distorta varied between 5.24% and 17.8% throughout the study. Infested male crabs ≥10.5 mm carapace width, which represented only 5.9% of the crabs collected, housed 68.8% of the total parasites recovered. Cryptoniscus larvae were much more frequent among molting (soft) than intermolt (hard) crabs. The cryptonisci infesting intermolt (hard) crabs were aggregated; i.e., they showed a contagious distribution. Females of L. distorta were actively breeding in spring and summer. In autumn, reproductive activity gradually decreased, and by winter, all the adult female parasites showed empty marsupia. The growth of immature parasites appears to stop in winter and resume in spring. The size of the adult marsupial female parasite was positively correlated with that of the host. Because only 1.1% of the mature female crabs carried marsupial parasites, it is unlikely that L. distorta plays a regulatory role in the reproductive potential of the host population.
... Research on this parasite has included its life history (Beck, 1980a;Anderson & Dale, 1981Anderson, 1990), prevalence (Chaplin-Ebanks & Curran, 2007;Key et al., 2011), and relationship with its shrimp hosts (Beck, 1980b, c;Anderson, 1990;Cash & Bauer, 1993;Bass & Weis, 1999;Chaplin-Ebanks & Curran, 2005;Sherman & Curran, 2013). Consumption of hemolymph by P. pandalicola can reach 10% of the total energy intake (Anderson, 1977) and up to 25% of total hemolymph volume of the shrimp on a daily basis (Walker, 1977). The physiological effects of this parasite on its host include sexual sterilization (Morris, 1948;Berg, 1979;John, 2011;Sherman & Curran, 2015), increased caloric intake (Anderson, 1977), decreased oxygen consumption and metabolic rate (Anderson, 1975) and decreased growth (Ludwig, 2009). ...
... It may be that growth in parasitized shrimp is affected by the bopyrid. Walker (1977) determined that one bopyrid parasite ingested enough grass shrimp hemolymph to constitute a significant loss to the host. Anderson (1975, 1977) found that the bopyrid parasite significantly affected P. pugio energetics to point of decreased respiration and metabolic activity (which may be the cause of shrimp reproductive sterility). ...
... This finding may in part be due to different energetic requirements as a result of bopyrid infection. Probopyrus pandalicola consumes hemolymph from its host at an average rate of 7-9 μl per day (Walker, 1977), and reduces the total energy intake of the shrimp by 1-10% (Anderson, 1977). To counteract this energy loss, infected shrimp generally consume more food than their unparasitized counterparts (Anderson, 1977), which was not an option in the present starvation study because shrimp had no access to food. ...
The daggerblade grass shrimp Palaemonetes pugio Holthuis, 1949 is prevalent in estuaries along the East and Gulf coasts of the United States, and is an integral part of the estuarine food web. Probopyrus pandalicola (Packard, 1879) is a bopyrid isopod that parasitizes P. pugio and decreases the energy available to its host by feeding on the hemolymph of the shrimp. The parasite also causes female shrimp to be castrated. The purpose of this study was to determine the effect of Probopyrus pandalicola on the survival time of P. pugio during starvation at two different temperatures. The experiment was conducted between September 2009 and June 2012 at 20.0 +/- 0.11 degrees C and 25.0 +/- 0.10 degrees C. Three trials at each temperature were performed. For each trial, parasitized, deparasitized and unparasitized shrimp were randomly placed into individual aquaria in a temperature-controlled chamber. All trials lasted until 100% shrimp mortality occurred. The bopyrid isopod did have a significant effect on shrimp survival times, but only at the higher temperature during which parasitized shrimp survived a significantly shorter amount of time (21.8 +/- 6.93 days) than unparasitized shrimp (25.2 +/- 8.25 days). In contrast, the bopyrid did not have a significant effect on shrimp survival times at the lower temperature, with shrimp surviving an average of 26.9-27.5 days. The results of this study have implications related to potential climate change, specifically higher temperatures, as we found that a small increase in temperature significantly affected the response of P. pugio to the isopod parasite. This supports prior research on other host-parasite interactions that are affected by increased temperature.
... En el curso de la mayoria de los crustaceos superiores la demanda energetlca durante la vitelogenesis secundaria es sin duda de mayo~ signi£icacion que en cualquiera de las etapas precedentes de la oogenesis (Adiyodi y Suhramoniam, 1983; Zerbib, 1979). De alii lo relevante de la privacion de nutrientes debida a los boporiidos (Walker, 1977) cita ingestas diarias de aproximadamente un 25 % del volumen de la hemolinfa del hospedador). Estos datos apuntalan la hipotesis del estron nutricional (Callan, 1940; Field, 1969; Calow, 1973; Adiyodi y Subramoniam , 1983). ...
... In most bopyrid isopod species the female bears little resemblance to a freeliving isopod, since it has severe modifications due to the parasitic life. The body is asymmetrical because it is adapted to the space that it occupies in the gill chamber or abdomen of the host; the pereiopods have been conserved but are ineffective for locomotion; the mouthparts have become a buccal cone used to penetrate the inner wall of the branchiostegite and suck the host hemolymph; and the ovaries occupy most of the female body (Walker, 1977;Overstreet, 1983;Markham, 1986;Janssen & Brandt, 1994;Boyko & Williams, 2009;Williams & Boyko, 2012). ...
Morphometric data are presented for developmental stages of Bopyrinella thorii (Richardson, 1904), obtained from 380 individuals of Thor floridanus Kingsley, 1878 infested by this parasite and collected by trawl net in Bahía de la Ascensión, Quintana Roo, Mexico. The close relationships between the sizes of host and parasite (r2 = 0.93) and between sizes of the two sexes of the parasite (r2 = 0.79) suggest the simultaneous growth of host and parasite and the permanence of the pairing of a male and female parasite throughout their lives. Cryptoniscus larvae of B. thorii were sometimes attached intramuscularly to other body parts than the host’s gill chambers. Mature females unpaired with a male had ovarian activity visible through their exoskeleton, which reveals that B. thorii could produce oocytes even in the absence of a male. Bilateral double infestation, present in 4.2% of the T. floridanus specimens analysed, was more frequent in smaller size classes of the host.
... p=0.72). Bopyrid isopods cause blood loss and effectively castrate their decapod crustacean hosts (Kuris 1974; Walker 1977; O'Brien and Van Wyk 1985), but are not expected to cause mortality. Since U. pugettensis is likely a novel host for O. griffenis and some bopyrids are not full castrators, we wanted to verify this relationship for this host/parasite system. ...
... Probopyrus pandalicola is a parasitic hematophagous isopod that infests palaemonid shrimp, including grass shrimp. The adult stage of this parasite lives in the shrimp's gill chamber, and forms a large deformation on the side of the host (Walker, 1977). ...
When exposed to methylmercury in the laboratory, grass shrimp, Palaemonetes pugio, parasitized by the isopod Probopyrus pandalicola, accumulated lower concentrations of mercury than their unparasitized counterparts. The parasitic isopod accumulated far less mercury than the grass shrimp. When exposed to mercury in a contaminated field site, mummichogs, Fundulus heteroclitus, parasitized with the nematode Eustrongylides, similarly accumulated lower concentrations of mercury than unpara-sitized fish, and the parasite similarly accumulated less than the host. The lower uptake by the parasites compared to their hosts is counter to the general view of biomagnification of methylmercury, since parasites are a trophic level above their hosts. The mechanism whereby parasitized animals accumulate less toxicant than unparasitized ones is unknown, but may be partially due to lower metabolic rate.
... Generally, the bopyrid isopods infest only one gill chamber of the host, and both female and male parasites can be found together. These parasites feed upon host hemolymph, and some species have been reported to consume a mean of 8% (Anderson, 1977) and up to 25% of hemolymph volume per day (Walker, 1977). In addition, the isopod female affects the gills respiratory efficiency, a condition that worsens in the presence of multiple infestations (McDermott, 1991). ...
The relationships between mean intensity and prevalence of infestation of Pseudione humboldtensis and the size and sex of the hosts, the squat lobsters Cervimunidia johni and Pleuroncodes monodon, from three fishing grounds in northern Chile are described. The prevalences were 13.6% and 6.8% for C. johni in Coquimbo and Huasco, respectively, while in P. monodon they were 18.2% and 0.6% in Coquimbo and Caldera, respectively. Between fishing grounds, no significant differences were found in the prevalence of infestation between male and female C. johni, but in Coquimbo, the prevalence of infestation in P. monodon was significantly higher in females. The sizes of infested squat lobsters were significantly lower than those of uninfested hosts. Males and females parasitized by P. monodon showed significantly lower body weights than uninfested hosts. Parasitized males of C. johni showed lower body weight than uninfested males. Only 0.6% of ovigerous females of C. johni and none of P. monodon were infested. The near absence of infested ovigerous females suggests castration process in females. A nonlinear relationship was detected between host size and parasite size for both females and males. Multiple infestations of P. humboldtensis were found in both host species, but they were more common in P. monodon. Given the high prevalence of multiple infestations (50%) and the significantly lower body weights of infested P. monodon, we suggest that this host is more vulnerable to P. humboldtensis than is C. johni.
... Female bopyrids feed with stylet-like mandibles that pierce the inner wall of the branchiostegite to suck hemolymph from their hosts (Walker, 1977). The mature female of L. distorta punctures a large horizontal vessel of U. uruguayensis before this vessel enters the pericardial sinus. ...
Fiddler crabs Uca uruguayensis were collected monthly in Punta Rasa, at the southern end of the Samborombón Bay, Río de la Plata, Argentina, from February, 1995, to March, 1996. Throughout the study, 1,115 of 12,033 crabs (9.3%) were infested by different developmental stages of the branchial bopyrid Leidya distorta, which is herein reported for the first time as infesting U. uruguayensis. The distribution of this parasite, previously known from New Jersey to Rio de Janeiro, is now extended even farther south, to the mouth of the Río de la Plata. Prevalence of L. distorta increased as a function of crab size. The newly settled cryptoniscus larvae were found in the space between contiguous gill lamellae after invading a previously uninfested branchial chamber. The cryptoniscus larva transformed into an early juvenile and, after molting one or more times, migrated to the roof of the branchial chamber, where it grew and finally reached the ovigerous condition. Female parasites usually carried cryptonisci or males, eventually both, on their bodies. Males were found in different positions on the females as the latter developed. Crabs housing a mature female parasite frequently bore an unpigmented area on the lateral wall of the branchial chamber. An additional faded area was sometimes observed on the bottom of the eye orbit. Adult female parasites usually produced a subtle lateral swelling on the carapace of the host, this deformation being more marked in smaller crabs than in larger ones. The major chela of the male crabs parasitized by adult females was, on average, 6.5% shorter than that of unparasitized ones. Alterations of the gills of the host were noticed: the adult female parasite had a strong dorsal carina that fitted between the fourth and fifth gills of the crab, displacing them laterally and making contact with the floor of the branchial chamber. The inner surface of the crab branchiostegite bore a large horizontal vessel from which the parasite presumably obtained hemolymph. Besides the bopyrid isopod forming the subject of this report, we found 61 crabs harboring a nematode larva, identified as Skrjabinoclava sp., among the internal organs of the crab.
... Females of bopyrids appear to suck large amounts of hemolymph from their hosts. Walker (1977) estimated that about a 25% of the hemolymph of Palaemonetes pugio Holthuis, 1949, is taken daily by Probopyrus pandalicola (Packard, 1879). The mature female of L. distorta punctures a large vessel of U. uruguayensis, which most likely provides abundant hemolymph for the parasite (see Roccatagliata and Torres Jordá, 2002). ...
On the basis of a sampling program performed monthly, a total of 12,033 fiddler crabs, Uca uruguayensis, were collected at the southern end of the Samborombón Bay, Río de la Plata estuary, Argentina, from February 1995 to March 1996. Density ranged from 133 to 207 ind/m2 over the 13-mo study period. The overall proportion of male crabs was 0.62. For small crabs, sex ratio was 1:1, but as crab size increased, sex ratio first became female biased and then male biased. Crabs carried eggs from mid-spring to late summer. Prevalence of the parasite Leidya distorta varied between 5.24% and 17.8% throughout the study. Infested male crabs ≥10.5 mm carapace width, which represented only 5.9% of the crabs collected, housed 68.8% of the total parasites recovered. Cryptoniscus larvae were much more frequent among molting (soft) than intermolt (hard) crabs. The cryptonisci infesting intermolt (hard) crabs were aggregated; i.e., they showed a contagious distribution. Females of L. distorta were actively breeding in spring and summer. In autumn, reproductive activity gradually decreased, and by winter, all the adult female parasites showed empty marsupia. The growth of immature parasites appears to stop in winter and resume in spring. The size of the adult marsupial female parasite was positively correlated with that of the host. Because only 1.1% of the mature female crabs carried marsupial parasites, it is unlikely that L. distorta plays a regulatory role in the reproductive potential of the host population.
... Bopyrid isopods cause blood loss and effectively castrate their decapod crustacean hosts (Kuris 1974;Walker 1977; O'Brien and Van Wyk 1985), but are not expected to cause mortality. Since U. pugettensis is likely a novel host for O. griffenis and some bopyrids are not full castrators, we wanted to verify this relationship for this host/parasite system.Smith et al. (2008)determined from field collections that O. griffenis caused significant weight loss in U. pugettensis but found the relationship to be variable and could not control for other possible factors like molting and feeding history. ...
A dramatic increase in prevalence of the recently discovered bopyrid isopod parasite, Orthione griffenis, likely introduced in the 1980s from Asia to the Pacific coast of North America, coincided with the 2002 collapse of a population
of its burrowing mud shrimp host, Upogebia pugettensis, in Willapa Bay, Washington that had been stable since monitoring began in 1988. An examination of whether O. griffenis infections were sufficient to cause this decline and other recently noted U. pugettensis population collapses in Pacific Coast estuaries was conducted. O. griffenis prevalence was the highest in large reproductive-sized female shrimp and caused an estimated average 68% loss of U. pugettensis reproduction in Yaquina Bay, Oregon over a 5-year period. O. griffenis prevalence fluctuated from year to year, but trends were similar in all estuaries sampled. Uninfected shrimp transplanted
back into locations from which they had disappeared acquired the parasite, suggesting that O. griffenis is extremely effective at finding its host even in estuaries with very low host density. Since both U. pugettensis and O. griffenis have pelagic larval stages, their population dynamics are also influenced by coastal nearshore oceanography and estuarine
recruitment success. Coastwide lack of estuarine recruitment appears to coincide with declines in density of a co-occurring
thalassinid shrimp, Neotrypaea californiensis, but cannot alone explain U. pugettensis population collapses. Although patterns observed to date could be explained by the presence of either a native or introduced
parasitic castrator, assumptions of a resilient co-evolved host–parasite relationship do not apply for introduced species,
so continued efforts to follow the spatial extent and consequences of the O. griffenis–U. pugettensis host–parasite relationship are warranted.
KeywordsParasitic castrator–Local extinctions–Introduced species–
Neotrypaea californiensis
–Thalassinidea
... Reinhard (1956) and Anderson (1977) highlighted the nutritional drain affecting PS energy flow, which could impair parasitized females of producing energy costly vitellogenic oocytes. Reinhard (1956), Baudoin (1975), Walker (1977) and Beck (1980) also discussed the possibility of endocrine mechanism disruption, by the reduction of circulating reproductive hormones (due to blood losses caused by parasites), stimulation of the gonad-inhibiting hormone (GIH) or even the secretion of GIH by bopyrids. The observations by Coutière (1899) on the alpheid shrimp Synalpheus biunguiculatus (Stimpson, 1860) and by Caroli (1930) on Synalpheus gambarelloides (Nardo, 1847) (=S. ...
The present work studied the degree of inhibition caused by the bopyrid isopod Eophryxus lysmatae (Caroli, 1930 [Caroli, E., 1930. Notizia di tre specie nuove ed una poco nota di Bopiridi addominali, parassiti di Caridei del golfo di Napoli. (Contributo alla conoscenza del genere Phrixus Rathke). Boll. Soc. Nat. Napoli 41, 258–269]), an abdominal parasite, on the reproductive performance of its host, the protandric simultaneous hermaphrodite shrimp Lysmata seticaudata (Risso, 1816). Parasitized shrimp (PS) was not able to produce embryos, although they could successfully fertilise the eggs of unparasitized shrimp (US). All US paired with PS were able to fertilise eggs when paired with other US. The average number of larvae (±S.D.) produced by US shrimp paired with US and PS (344±27 and 346±23, respectively) was not significantly different (p=0.73). The average intermolt period duration (±S.D.) for US and PS (10±1.2 and 11±0.8 days, respectively) was not significantly different (p=0.82), with bopyrid parasites molting synchronously with their host. No PS lost its parasite during ecdysis. Although only three parasitized shrimp were used in the present work, parasitic castration induced by E. lysmatae seems to only affect the female sexual system of the simultaneous hermaphrodite L. seticaudata, and therefore parasite-induced “reproductive death” does not occur in this species as in other gonochoric and sequencial hermaphroditic caridean shrimp. Nutritional drain and disruption of endocrine mechanisms possibly caused by the bopyrid parasite are discussed.
In the symbiosis between ghost shrimps and bopyrid isopods we studied some reciprocal effects on the reproduction of the symbionts. Samples were taken between february and july 1995 at Lenga, Chile (36 degrees 45' S; 73 degrees 10' W). Hosts were sampled from two habitats: estuary and beach, and consisted on 214 Callichirus garthi (Retamal 1975) and 497 Neotrypaea uncinata (Edwards, 1837). The distribution, abundance and fecundity of isopods in shrimps were compared among habitats and species. Also, we studied the correlation between the isopod body size and the host body size, as well as the relationship between isopod body size and its fecundity. We evaluated the effect of isopods on the host reproduction by comparing the gonadic maturity and the morphometry of sexual secondary characters in parasitized and isopod-free shrimps. The ghost shrimp N. uncinata was the only parasitized species: Ionella agassizi Bonnier 1900 accounted for 98.8% of the 324 isopods collected. The other isopod species was Ione ovata Shiino 1964. prevalence increased with host body length and large shrimps harboured bigger isopods, which instead had higher fecundity. We found that the beach shrimps were less parasitized than the estuary shrimps. However, the host's habitat was not as important in the isopod fecundity as the host body size. I. agassizi affected glaringly the host reproduction, because prevented ovarian maturation and the secondary sexual characters of the parasitized shrimps were smaller than in unparasitized ones. This is interpreted as resulting from the high nutritional interference by the parasitic isopod on its host.
This study describes the prevalence of a parasitic bopyrid isopod, Pampenaeon consolidatum, on Metapenaeopsis dalei and its effect on host growth and reproduction. The prevalence of P. consolidatum increased with shrimp size, from 27.3% at 5 mm CL to 68.4% at 16 mm CL. Lengths of female bopyrids and that of their hosts were positively correlated. This indicated that the bopyrid stays continuously with its host and is not detached when the host molts. Morphometric analyses indicated that parasitized male and female shrimp have slightly lower body weight and length than nonparasitized shrimp of the same carapace length. The gonadosomatic index was higher for nonparasitized than for parasitized female shrimp. Growth of the petasma, the copulatory organ of male shrimp, was significantly affected by the parasite.
The bopyrid isopod Probopyrus pandalicola is a hematophagous ectoparasite that sexually sterilizes some palaemonid shrimps, including female daggerblade grass shrimp Palaemonetes pugio. The reproduction of parasitic isopods is thought to occur synchronously with host molting because the brood would be unsuccessful if molting occurred before the larvae were free swimming. Temperature affects the length of the molting cycle of shrimp, and therefore may also affect the incubation time of isopod broods. The purpose of the present study was to determine the effect of temperature on brood development of the parasite and on synchronization with the molting of its host. Parasitized P. pugio were monitored daily at 2 experimental temperatures, 23 C and 15 C, in temperature-controlled chambers for the duration of a full parasite reproductive cycle. Developmental stage was determined by the visible coloration of the brood through the exoskeleton of the host, and was designated as egg, embryo I, embryo II, or epicaridium larvae. Temperature significantly affected median brood incubation time, which was only 11 days at 23 C, as compared to 35 days at 15 C. The final developmental stage (epicaridium larvae) was 3 times shorter at 23 C (median 3 days; n=45) than at 15 C (median 9 days; n=15). Temperature significantly affected the intermolt period of parasitized shrimp, which was shorter at 23 C (median 12 days) than at 15 C (median 37 days). A smaller percentage of the intermolt period elapsed between larval release and shrimp molting at 23 C (0.0%) than at 15 C (3.1%), indicating closer synchronization between host molting and parasite reproduction at the warmer temperature. At 15 C the isopods utilized a smaller proportion of the time that was available for brood incubation during the intermolt period of their host. Brood size ranged from 391 to 4,596 young and was positively correlated with parasite and host size. Since development progressed more rapidly at 23 C, warmer temperatures could increase the prevalence of P. pandalicola. The corresponding reduction in the abundance of ovigerous grass shrimp as a result of sexual sterilization by bopyrids could adversely impact estuarine ecosystems, as grass shrimp are a crucial link in transferring energy from detritus to secondary consumers.
ABSTRACT Of 558 Palaemonetes spp. exposed to infective cryptoniscus larvae of Probopyrus pandalicola, 364 became infected (most within 24 h after exposure). Larvae of Probopyrus pandalicola are host specific (permanent infections leading to parasite maturation resulted when Palaemonetes pugio was exposed but only temporary infections or host death resulted when Palaemonetes vulgaris was used). Parasite success was also dependent on host age: young hosts of both species became infected more readily than older ones. Parasites typically are endoparasitic for up to 2 weeks after infection, later becoming ectoparasitic in the branchial chamber. However, the endoparasitic stage is unnecessary for parasite larvae infecting hosts already harboring a female bopyridium within the branchial chamber. Often, loss of parasites from hosts or movements of parasites after infection (i.e., during the transition from endoparasitism to ectoparasitism or during movement from one branchial chamber to the other) occurred at host ecdysis. The mortality rate of experimentally infected hosts is high during the parasite's endoparasitic stage which lasts from 1-2 weeks. However, the mortality rate 5 weeks after infection is near that of uninfected shrimp. Although my results suggest that parasites were distributed at random among shrimp in exposure vessels, further studies of parasite distribution using larger experimental host populations are warranted.
The mud shrimp Upogebia major (Upogebiidae: Decapoda: Crustacea) is a common species on muddy and sandy mud tidal flats in the west coast of Korea. They reside in Y-shaped burrows that can extend up to more than 2 meters below the sediment surface. They feed on suspended detritus carried into their burrow by the beating of their pleopods and captured by their hairy first two pairs of thoracic legs. Mud shrimp burrows provide a habitat for a variety of small organisms such as crabs, shrimps, polychaetes, and mollusks. Ovigerous females are observed from December to May. Females deposit eggs only once per breeding season. They start hatching in March and the pelagic larvae of first zoea appear in March and April, followed by benthic settlement in May. Growth over the first year is rapid, and females deposit their first eggs in the third breeding season, 31 months after their settlement. Adult shrimps live for 4~5 years. Depth of the burrow increases with body length. The deep burrows provide refuge from predators and physical stress, allowing the shrimps to survive for a long time. The mud shrimps supply oxygen-rich water to their deep burrows, and exert a great influence on the structure and metabolism of the tidal flat benthic community. However, recently this type of mud shrimp has posed a serious threat to the Korean clam industry along the west coast of Korea. The extensive burrowing shrimp populations suddenly invaded the tidal flats from 2010 where the clams (Ruditapes philippinarum) are raised. As a consequence, clam production has decreased by about 10% over the past three years in some Korean clam beds. Therefore, the objective of this study is to review the biology of this mud shrimp in order to seek solutions to control the burrowing of these shrimps.
This study describes changes in the secondary sexual characters of Thor floridanus Kingsley, 1878 males, caused by the isopod Bopyrinella thorii (Richardson, 1904). Of 380 specimens of T. floridanus examined, the females were more often infested (n = 313) than the males (n = 41), and had a wider size range (0.7-2.85 mm POCL) compared to the males (0.9-2.32 mm POCL); no ovigerous females of T. floridanus were found. In 25 males the appendix masculina was reduced in size, the endopod of the second pleopod was barely ornamented, and the flexor margin of the propod of the third pereiopod was similar to that of the female of the species; all those males were classified as “feminized”. Those individuals were infested mainly by pairs of mature parasites, and 75% of the “primary” males carried cryptoniscus larvae, suggesting that the “feminization” of the males is caused by the parasite, as a result of the sexual development of hosts and parasites.
Several Probopyrus ssp. produce ecto- and endoparasitic (tissue) larvae. The purpose of this paper is to evaluate the colonization and distribution of cryptoniscus larvae in shrimp of both sexes and to perform a microanatomical analysis of the larvae-bearing tissue in order to typify the tissues involved and their eventual reaction. The following conclusions are drawn: (1) ecto- and endoparasitic cryptoniscus colonize the various body areas of Palaemonetes argentinus at random, affecting young shrimp, maturing shrimp, and sexually mature shrimp; (2) only the ectoparasitic larvae that reach the branchial chamber become actually integrated to the consortium; (3) the tissue larvae are erratic guests of the shrimp's connective-hemolymphatic tissue and no tissue reaction leading to the isolation of the larvae occurs and this is not the result of a systemic immunological depression in the host; (4) the tissue cryptonisci located next to the gonad of shrimp of either sex do not have any effect on the normal development of germinal cells.
1.1. The relationship between host and parasite rates of energy metabolism was used to estimate the energy burden of Argeia pauperata on its host Crangon franciscorum.2.2. Respiration rates of the host were not significantly affected by the parasite even though the caloric turnover rate of the parasite was more than three times that of the host.3.3. The ratios of both energy expenditure and size of the parasite to those of the host were positively correlated with host size.
Thirteen species of parasitic bopyrid isopods occur on New Zealand decapod crustaceans. Six species: Pseudione pontocari; P. murawaiensis; Gyge angularis; Gigantione pikei; Rhopalione atrinicolae; and Pseudostegias otagoensis are new to science. Five species: Pseudione affinis (Sars); P. hyndmanni (Bate & Westwood); Pleurocryptella infecta Nierstrasz & Brender à Brandis; Hemiarthrus nematocarcini Stebbing; and Eophrixus shojii Shiino are recorded for the first time in New Zealand. The 2 remaining species, Pseudione hayi Nierstrasz & Brender à Brandis and Athelges lacertosi Pike are previously described endemics. These 13 species belong to 4 of the 10 currently recognised subfamilies of the Bopyridae. The new species are described, and all species are figured.
A population approach was employed to study the effects of a bopyrid isopod, Aporobopyrus muguensis, on the growth and reproduction of its anomuran host, Pachycheles rudis. Indirect evidence, provided by the size-specific prevalence pattern, and direct evidence, provided by laboratory moult frequencies and moult-stage data, indicated that the frequency of moulting was reduced among parasitized crabs. Moult increments of parasitized crabs were less than those of non-parasitized crabs. Although parasitized female P. rudis were able to reproduce, their fecundity was substantially reduced. Parasitized female hosts appeared to be delayed in their attainment of sexual maturity. Once mature, these crabs produced significantly smaller size-specific clutches than those produced by non-parasitized female crabs. Because fecundity increases with size in P. rudis, the slower growth rates of parasitized female hosts may further limit their fecundity. Potential mechanisms by which A. muguensis limits the growth and reproduction of P. rudis are discussed.(Accepted March 22 1982)
Freshwater shrimp, Palaemonetes paludosus, infected by the bopyrid isopod, Probopyrus pandalicola, occurred as far as 33 km upstream in many coastal rivers and canals throughout Florida. Free-swimming isopod larvae and the intermediate copepod host, Acartia tonsa, were collected in the plankton of the Wakulla River, and it appeared that cryptoniscus larvae swam at least as far as 13 km upstream to infect the definitive shrimp host after leaving the copepod in brackish water. In the Wakulla River infection levels ranged from 87·5 to 100%. In contrast, at McBride's Slough infection levels fluctuated from 0·9 to 93·2%. In the St Marks River the frequency of infected shrimp gradually increased from 0% upstream to 96%, 6 km further downstream. A significantly greater percentage of female than male hosts were infected, but only females of size classes less than 31 mm long had a greater frequency of infection. Female P. pandalicola were greatly under-dispersed (coefficient of dispersion (s2/x¯) less than 1) throughout the host population; 99·6% of the infected hosts carried only 1 female parasite. Control of P. pandalicola at the infrapopulation level is probably accomplished by some mode of intraspecific competition, and control at the suprapopulation level occurs through an upstream limitation of the transmission range of the cryptoniscus larval stage. Host–parasite interactions appear to be unstable.
The behaviour of two ectosymbiotic animals, Peregrinamor
ohshimai (a bivalve attached to the ventral cephalothorax of the host), and Phyllodurus sp. (a bopyrid isopod attached to the second pleopod of the host), during ecdyses of the host thalassinidean Upogebia shrimps was studied by time-lapse video of infested shrimps. In the intermoult stages of the hosts, both ectosymbionts did not move. However they moved on to the newly emerged body of the host at the time when the host moulted. Peregrinamor
ohshimai began to move just after the host started moulting, whereas Phyllodurus sp. moved prior to ecdysis of the host and waited near the fissure from which the newly moulted body emerges first. There are highly correlated morphological relationships between the symbionts and the hosts. It is suggested that both ectosymbionts grow with the same host individuals after infection, keeping morphological affinity with their hosts without being discarded during ecdyses of the hosts.
When exposed to methylmercury in the laboratory, grass shrimp, Palaemonetes pugio, parasitized by the isopod Probopyrus pandalicola, accumulated lower concentrations of mercury than their unparasitized counterparts. The parasitic isopod accumulated far less mercury than the grass shrimp. When exposed to mercury in a contaminated field site, mummichogs, Fundulus heteroclitus, parasitized with the nematode Eustrongylides, similarly accumulated lower concentrations of mercury than unparasitized fish, and the parasite similarly accumulated less than the host. The lower uptake by the parasites compared to their hosts is counter to the general view of biomagnification of methylmercury, since parasites are a trophic level above their hosts. The mechanism whereby parasitized animals accumulate less toxicant than unparasitized ones is unknown, but may be partially due to lower metabolic rate.
The isopod Notophryxus lateralis is ectoparasitic on the euphausiid shrimp Nematoscelis difficilis in the Santa Barbara Channel, California. It infects 0.24% of the host population. The parasite has not previously been reported on this host. Color and respiratory movements of live parasites are noted. Various larval stages are described. The isopod causes parasitic castration of male and female euphausiids, the effect being a reduction in size of testis or ovary. Males appear incapable of spermatophore or spermatotheca production, while females show reduction in oocyte size and some cytologic dedifferentiation. Parasitic castration by isopods has been reported only for the family Bopyridae, which infects intertidal or subtidal crustaceans.
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1.1. The blood proteins of Crangon consist of haemocyanin (60–93 per cent of total protein) and minor proteins (characterized as apophaemocyamines, esterases and glycoproteins after starch gel or fluid agar electrophoresis).2.2. These proteins may vary tenfold in their concentration, but this variation is significantly correlated with the moulting cycle and, to a lesser extent, with season.3.3. During starvation, the blood proteins, particularly the glycoprotein fraction, fall in concentration. These changes are reversed by feeding. Concomitant changes in blood [Cy] are also seen.4.4. During starvation, the hepatopancreas accumulates Cu from the blood into copper vesicles. It is suggested that the hepatopancreas could accept all the copper circulating in the blood should haemocyanin be completely broken down.5.5. It is concluded that the observed copper and protein changes in brachyurans such as Maia during the moult cycle may be compared with natantians only when the effects of obligatory starvation in the former are taken into account.
Measurements of incorporation of 14C from differentially labelled glucose and pyruvate into uterine lipid and CO2 were used to evaluate early metabolic changes produced by estradiol in immature rat uterus. Tissue was incubated with the isotopes in vitro after hormone treatment in vivo. With pyruvate-3-14C as substrate, substantially more 14CO2 is produced than with glucose-1-14C or glu-cose-6-14C as substrates. Also, 14CO2 output from glucose-1-14C is about double that from glucose-6-14C. Estradiol treatment causes a similar increase of 14C incorporation into lipid with either of the glucose substrates or with pyruvate. This suggests that the estradiol effect on lipid synthesis is beyond pyruvate. A differential effect on 14CO2 production from glucose and pyruvate, however, locates an estradiol effect between these substrates. Furthermore, the estradiol acceleration of 14CO2 production from glucose-1-14C and glucose-6-14C is equal. This suggests that the site of estrogen stimulation of uterine glucose metabolism is prior to the formation of glucose-6-phosphate and therefore implicates the transport step, the phosphorylation step, or both.